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Use of incidentally encoded memory from a single experience in cats

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Abstract

We examined whether cats could retrieve and utilize incidentally encoded information from a single past event in a simple food-exploration task previously used for dogs (Fujita et al., 2012). In Experiment 1, cats were led to four open, baited containers and allowed to eat from two of them (Exposure phase). After a 15-min delay during which the cats were absent and all containers were replaced with empty ones, the cats were unexpectedly returned to the room and allowed to explore the containers (Test phase). Although the cats' first choice of container to visit was random, they explored containers from which they had not previously eaten for longer than those from which they did previously eat. In the Exposure phase of Experiment 2, two containers held food, one held a nonedible object, and the fourth was empty. Cats were allowed to eat from one of them. In the post-delay Test phase, the cats first visited the remaining baited-uneaten container significantly more often than chance and they spent more time exploring this container. Because the cats' behavior in the Test phase cannot be explained by association of the container with a pleasant experience (eating), the results suggest that cats retrieved and utilized "what" and "where" information from an incidentally encoded memory from a single experience.

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... Cats have good long-term memory and can remember a single event, such as a negative experience during a veterinary visit. 12 not only affect the cat at that time but will also influence their emotional responses and behaviors at subsequent veterinary visits. [12][13][14] Classical conditioning will lead to emotional associations with the veterinary experience even when there has not been any one specific negative experience. ...
... 12 not only affect the cat at that time but will also influence their emotional responses and behaviors at subsequent veterinary visits. [12][13][14] Classical conditioning will lead to emotional associations with the veterinary experience even when there has not been any one specific negative experience. For example, if a cat is painful or fearful during a veterinary visit, which may be as a result of their physical health condition, that protective emotional bias will become associated with the veterinary context and the cat may, therefore, respond protectively at future visits. ...
... Starting off with cat friendly interactions during kittenhood can help prevent negative responses in the future. [12][13][14] Neonates and pediatrics (0-12 weeks) While traditionally it might have been considered normal practice to scruff pediatric and neonatal feline patients, due to their size and demeanor, scruffing is no longer recommended for cats at any life stage. it is a mistaken premise that scruffing makes patients easier to work with. ...
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Practical relevance The ‘2022 AAFP/ISFM Cat Friendly Veterinary Interaction Guidelines: Approach and Handling Techniques’ (hereafter the ‘Cat Friendly Veterinary Interaction Guidelines’) support veterinary professionals with feline interactions and handling to reduce the impact of fear and other protective (negative) emotions, in so doing enhancing feline welfare and In implementing these Guidelines, team satisfaction and cat caregiver confidence in the veterinary team will increase as the result of efficient examinations, better experience, more reliable diagnostic testing and improved feline wellbeing. Veterinary professionals will learn the importance of understanding and appropriately responding to the current emotional state of the cat and tailoring each visit to the individual. Clinical challenges Cats have evolved with emotions and behaviors that are necessary for their survival as both a predator and prey species. A clinical setting and the required examinations and procedures to meet their physical health needs can result in behavioral responses to protective emotions. Cat friendly interactions require understanding, interpreting and appropriately responding to cats’ emotional states and giving them a perceived sense of control while performing the required assessment. Evidence base These Guidelines have been created by a Task Force of experts convened by the American Association of Feline Practitioners and the International Society of Feline Medicine, based on an extensive literature review and, where evidence is lacking, the authors’ experience. Endorsements These Guidelines have been endorsed by a number of groups and organizations, as detailed on page 1127 and at catvets.com/interactions and icatcare.org/cat-friendly-guidelines .
... Several other studies have investigated animal's capacity to incidentally encode information (e.g., Goldberger et al., 1980;Fujita et al., 2012;Fugazza et al., 2016Fugazza et al., , 2020Takagi et al., 2017;Sluka et al., 2018;Allen et al., 2020), however, often the to-be-remembered item is the centre of attention at the time of encoding (i.e., the animals are trained with the object of the incidental encoding) and it is possible that animals deliberately encoded it instead of incidentally (for further discussion on this subject, see Chapter 2, Eurasian jays show sex differences in simple discrimination learning and incidental encoding of the thesis). Thus, it would be relevant to propose a new way of testing incidental encoding in animals, where the object to incidentally encode is not the focus of attention during training. ...
... Zentall first raised the issue in pigeons (Zentall et al., 2008). Subsequently, several studies were run on dogs (Fujita et al., 2012;Fugazza et al., 2016;Sluka et al., 2018), cats (Takagi et al., 2017), squirrel monkeys (Goldberger et al., 1980), and rats (Zhou et al., 2012;Allen et al., 2020). In these studies, the to-be-remembered item is the centre of attention at the time of encoding, but the animal is supposedly not aware that their memory will be tested. ...
... In these studies, the to-be-remembered item is the centre of attention at the time of encoding, but the animal is supposedly not aware that their memory will be tested. In the study of Fujita et al., (2012) later adapted by Takagi et al., (2017) and Sluka et al., (2018), dogs and cats were presented with trays disposed in a fan shape and were allowed to eat from two of them. At test, the animals had the opportunity to explore similar trays, and the first tray revisited by animals was recorded (Fujita et al., 2012;Takagi et al., 2017). ...
Thesis
Some authors support that mental time travel is unique to humans. To their point of view, animals are not able to project themselves into the past of the future because they are bound into the present. Nevertheless, during the last 30 years, researchers have brought considerable knowledge on animals’ capacities to travel mentally through time. Even though opinions have evolved, the debate concerning the unicity of mental time travel is still on. My PhD thesis aimed at bringing further knowledge on this matter by focusing on an innovative aspect of episodic cognition in common cuttlefish, Sepia officinalis and Eurasian jay, Garrulus glandarius, namely, source-memory. Source-memory is the capacity to retrieve the origin of an episodic memory. Results showed that cuttlefish were able to perform a source-discrimination study, revealing that they were able to discriminate and retrieve their own perceptions after 3-hours delay. A study on jays’ capacity to encode incidentally a contextual information (contextual source) revealed unexpected differences between males and females. Investigation of future-oriented behaviour in cuttlefish showed that they were able to take a decision in the present according to previous encoded knowledge and according to future experimental conditions. A preliminary study also revealed promising results on cuttlefish capacity to anticipate their future needs. To finish, we explored and revealed for the first time the neuronal substrates of episodic-like memory in cuttlefish. Alltogether, these results provide new knowledge on mental time travel in cuttlefish and in jays, suggesting that this capacity would have evolved under different environmental contraints.
... Research on feline memory has lead to the finding that cats can easily equal dogs in cognitive tests [84] however the way in which their memory works differs. We will discuss both long-term and short-term memory here. ...
... This means that cats can utilise what and where information from an incidentally encoded memory of a single experience. This is similar to episodic memory which is made up of two types -WWW memory (memory which deals with What, Where, and When something happened), and incidental memory (memory which is stored subconsciously) [84]. ...
... With regards to feline memory, which is discussed in Section 2.3.2, studies have shown that cats can equal dogs in cognitive tests [84]. It was in fact found that long-term memory is quite advanced for cats [15,18]. ...
Thesis
The affects of the combination of game (and toy) design and Animal Welfare Informatics has been studied and applied in relation to multiple species; categorised into domesticated, wild, shelter, zoo, circus, and factory farmed animals. By observing current research, it may easily be deduced that the majority of such research has been conducted in relation to domestic dogs. The domestic dog (canis familiaris) has been part of the daily lives of humans for thousands of years, however this same statement may be applied to the domestic cat (felis silvestris catus or felis catus) as well. On a global scale, domestic cats actually outnumber domestic dogs. However, comparatively, most of animal-centred research has focused on dogs. A major reason for this is that researchers believe that cats are uncooperative which is not always the actual case. Both domesticated species should be given importance so as to aid in their welfare. In fact, all of the differently categorised species should be given such importance. That being said, this is not the incentive behind this dissertation. Certain elements which will be delved into may however prove to be applicable to these other species. The motivation behind this dissertation is the fact that, similar to domestic dogs, domestic cats may suffer from cognitive decline due to a combination of a progression of age and a lack of mental stimulation. Over the years, several playful artefacts-from intelligent toys to digital games-have been developed for domestic dogs to lessen this cognitive decline but unfortunately, no such games have yet been designed for domestic cats. The objective of this dissertation is thus to provide a basis for the design of a playful artefact which, after its future development, will potentially alleviate cognitive decline in domestic cats. Originally however, the main objective behind this dissertation was to design and develop a digital memory game to possibly alleviate cognitive decline in domestic cats. This changed in time due to several analyses of background information as well as my own deductions and personal reflections. This research ended up being centred around the analysis of any existing related research , and the proposition of a set of game design guidelines in the context of feline cognitive decline following the existing research. Part of this contribution of knowledge centred around the introduction of game concept documents which were based on the research and proposed guidelines, the discussion of how each concept was formulated, and the corresponding comparatory analysis. To explain this in more detail, a set of twenty-two guidelines were proposed and applied to design two separate concept documents-one for a non-digital system and the other for a digital system. The comparatory analysis of these two concepts resulted in the conclusion that, while both systems have potential, it may be safer in the long run to develop the non-digital system (at the current time frame of this dissertation). This result stemmed mostly from the fact that the digital system's concept did not make use of all of the guidelines due to the current technological availability, and that we had no means of accurately testing whether the act of not implementing all of the guidelines would negatively impact the domestic cat or not. After all, the domestic cat's welfare is given top priority in this research. Future work following this research may involve (but is not limited to) the development of the proposed non-digital system, the development of the proposed digital system, a series of practical tests or playthroughs of the developed system/s on some domestic cats, recording of data from the conducted practical tests, and possible iterations of design and development for the system/s based on the acquired test results.
... Since its emergence [79], researchers have used the incidental encoding and unexpected question paradigm to explore episodic-like memory in various non-human animals, including pigeons [79][80][81], rats [74,82,93,94], dogs [95][96][97], cats [98], corvids [92] and dolphins [83]. These studies demonstrate that multiple non-human species are able to encode and recall incidental information within remembered events, such as spatial locations [80,81,83,93,97,98], visual markers [92], the identity of experimenters [83], the presence (or absence) of food [74,82], odour cues [94], as well as aspects of their own [79][80][81]93,95] and other's behaviour [96]. ...
... Since its emergence [79], researchers have used the incidental encoding and unexpected question paradigm to explore episodic-like memory in various non-human animals, including pigeons [79][80][81], rats [74,82,93,94], dogs [95][96][97], cats [98], corvids [92] and dolphins [83]. These studies demonstrate that multiple non-human species are able to encode and recall incidental information within remembered events, such as spatial locations [80,81,83,93,97,98], visual markers [92], the identity of experimenters [83], the presence (or absence) of food [74,82], odour cues [94], as well as aspects of their own [79][80][81]93,95] and other's behaviour [96]. By focussing on a separate aspect of human episodic memory to the what-where-when memory paradigm, these studies develop an alternative methodology to investigate episodic-like memory and thus have the potential to strengthen previous findings (e.g. ...
Article
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Episodic memory involves the conscious recollection of personally experienced events and when absent, results in profound losses to the typical human conscious experience. Over the last 2.5 decades, the debate surrounding whether episodic memory is unique to humans has seen a lot of controversy and accordingly has received significant research attention. Various behavioural paradigms have been developed to test episodic-like memory; a term designed to reflect the behavioural characteristics of episodic memory in the absence of evidence for consciously experienced recall. In this review, we first outline the most influential paradigms that have been developed to assess episodic-like memory across a variety of non-human taxa (including mammals, birds and cephalopods), namely the what–where–when memory, incidental encoding and unexpected question, and source memory paradigms. Then, we examine whether various key features of human episodic memory are conceptually represented in episodic-like memory across phylogenetically and neurologically diverse taxa, identifying similarities, differences and gaps in the literature. We conclude that the evidence is mixed, and as episodic memory encompasses a variety of cognitive structures and processes, research on episodic-like memory in non-humans should follow this multifaceted approach and assess evidence across various behavioural paradigms that each target different aspects of human episodic memory. This article is part of the theme issue ‘Elements of episodic memory: lessons from 40 years of research’.
... Tests to evaluate working memory for hidden food were first administered to domestic cats with a maximum retention interval of 60 seconds 82 . More recently, Takagi et al. 77 studied working memory in domestic cats with a delay phase of approximately 15 minutes (a range of 12-23 minutes): subjects were required to retrieve and utilize incidentally encoded information from a single past experience in a simple food-exploration task. While Fiset and Doré 82 showed that cats' working memory declines between 10 and 30 seconds, results from Takagi et al. 77 suggested that cats could retrieve not only "where" information but also "what" information from a single past event for much longer periods, even beyond the previously believed working memory capacity of cats for retaining information. ...
... More recently, Takagi et al. 77 studied working memory in domestic cats with a delay phase of approximately 15 minutes (a range of 12-23 minutes): subjects were required to retrieve and utilize incidentally encoded information from a single past experience in a simple food-exploration task. While Fiset and Doré 82 showed that cats' working memory declines between 10 and 30 seconds, results from Takagi et al. 77 suggested that cats could retrieve not only "where" information but also "what" information from a single past event for much longer periods, even beyond the previously believed working memory capacity of cats for retaining information. The other important factor for choosing an appropriate cognitive test for cats is the test's sensitivity to cover aspects of domestic cat cognitive function. ...
Article
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Background: Age-related dementia has been documented in domestic cats; however, its interaction with naturally occurring feline immunodeficiency virus (FIV) infection has been investigated minimally. Methods: Visuospatial working memory (VSWM) and problem-solving (PS) ability were evaluated in FIV-infected (n = 37) and control cats (n = 39) using two cognitive tasks tested serially, which assessed the ability of cats to remember the location of a baited container after a set delay, then evaluated the capability of the cats to manipulate the container to obtain the food within a time limit. Cats were categorized using 7 years of age as a cut-off to determine age-related differences. The relationship between cognitive performance and FIV viral load was investigated using real-time PCR cycle threshold (Ct ) values. Results: Age significantly affected VSWM and PS ability. Younger cats had better VSWM performance and PS ability compared to older cats with the same FIV status. There was no difference between younger FIV-positive and negative cats in either part of the task. While older FIV-positive cats had significantly worse VSWM than older FIV-negative cats, no differences were found in PS ability. Additionally, Ct values predicted VSWM but not PS ability. Conclusion: Age-related cognitive impairments and FIV infection appear synergetic, causing greater cognitive deficits in older FIV-infected cats.
... We expanded the study to include cats, as little is known regarding cat cognition despite the similarities between cats and dogs-both are carnivorous mammals that have been selectively bred and domesticated by humans and kept as companions (see Vitale Shreve and Udell, 2015 for a review on cat cognition). Furthermore, a paradigm originally designed to test dogs' memory of an event found that cats can also remember what and where information from a single episode (Takagi et al., 2017), indicating possible similarities between event memories in cats and dogs. ...
... Both cats and dogs reportedly remembered events that occurred many months ago. Dogs can recall memories from weeks ago (Demant et al., 2011), but as far as we are aware, the longest delay observed in cats has been minutes (Okujava et al., 2005;Takagi et al., 2017), although see Saito and Shinozuka (2013) for an example of long-term recognition in cats. Furthermore, the retention periods we were able to observe necessarily were limited to the duration in which participants had owned their pet. ...
Article
The case for episodic memory in non-human animals has been intensely debated. Although a variety of paradigms have shown elements of episodic memory in non-human animals, research has focused on rodents, birds and primates, using standardized experimental designs, limiting the types of events that can be investigated. Using a novel survey methodology to address memories in everyday life, we conducted two studies asking a total of 375 dog and cat owners if their pet had ever remembered an event, and if so, to report on their pet’s memory of the event. In both studies, cats and dogs were reported to remember a variety of events, with only 20% of owners reporting that their pet had never remembered an event. The reported events were often temporally specific and were remembered when commonalities (particularly location) occurred between the current environment and the remembered event, analogous to retrieval of involuntary memories in humans.
... Regarding the non-randomization of the test order, we chose to perform the stress-free test first to avoid negative memory association with the execution of the STT-1 with stress, as cats can exhibit episodic-like memory. 29,30 Conclusions The findings of this study suggest that acute stress may increase tear production in cats; however, the STT-1 values obtained during the stress-inducing intervention were within the normal range. In addition, it was observed that the use of cat friendly handling techniques facilitated the examination, keeping the animals calmer during the procedure. ...
Article
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Objectives This study aimed to determine the impact of acute stress on tear production in companion cats to provide a basis for minimizing stress-inducing stimuli during ophthalmic evaluations. Methods A total of 24 healthy owned cats (12 males, 12 females) of mixed breed, aged 8 months to 7 years, with no history of ocular diseases, were selected for the study. The cats were housed in individual cages under controlled conditions for 6 days. The Schirmer tear test-1 (STT-1) was performed in the morning (between 9:00 am and 11:00 am) using test strips from the same batch. The first test (without stress) was conducted on the fifth day of acclimation, and the second test (with stress) on the sixth day. The stress stimulus consisted of recordings of barking dogs, cats fighting and the murmuring of people. For both tests, the heart rate was assessed with a stethoscope before, during and after the tests, and the environmental stress level was also evaluated. Results are presented as mean ± SD and 95% confidence interval (CI). Results The study found that STT-1 values were significantly higher ( P = 0.009) with stress (22.2 ± 6.0 mm/min [95% CI 19.9–24.6]) than without stress (17.5 ± 6.9 mm/min [95% CI 14.8–20.2]). Similarly, the heart rate was significantly higher ( P = 0.028) in stress vs non-stress conditions (213.4 ± 37.5 beats per minute [bpm] [95% CI 198.7–228.1] vs 171.5 ± 28.6 bpm [95% CI 160.3–182.7], respectively), and the environmental stress score was significantly higher ( P <0.001) in stress vs non-stress conditions (3.3 ± 0.5 [95% CI 3.1–3.5] vs 1.2 ± 0.4 [95% CI 1.1–1.4], respectively). Conclusions and relevance Stress increased tear production in cats. Although the mean STT-1 value obtained under stress conditions was within the normal range, stress can influence the test results. The use of cat friendly handling techniques facilitates execution of the STT-1.
... Studies performed in corvids [6] and rats [7,8] indicated that these animals were also capable of using behavior criteria derived from episodic memory about past events, regardless of whether they have self-consciousness; this occurrence is called "episodic-like" memory [6][7][8][11][12][13][14][15]. Further studies were performed in primates [5,9,11,18], cats [24], fishes [25], cuttlefish [26] and domestic dogs [10,19,27], revealing the presence of episodic-like memory in these species. ...
Article
Episodic memory, in humans, is the memory most affected by age-related deterioration or the constitution of neurodegenerative pathologies, such as Alzheimer's disease. However, it is unknown whether this relationship is also present in nonhuman animals. Since studies in birds, rats, primates, and dogs have been shown to have episodic-like memory, more studies aiming to improve the present understanding of this relationship in nonhuman animals are important to aid the development of new translational models for neurodegenerative disorders. Knowing that dogs (Canis familiaris) represent a promising experimental model for neurodegenerative disorders, a memory retrieval test was conducted with 90 clinically healthy domestic dogs of different ages, both sexes, and distinct breeds, for the purpose of evaluating episodic-like memory. The present study adapted a test that corroborates episodic memory requirements through incidental codification of experienced events. We performed a test with two exposure phases, with different characteristics between them, so that in the third phase it was necessary to integrate previous experiences in order to achieve success in the test. In our study, it was possible to verify the decline of episodic memory in elderly dogs, even clinically healthy, regardless of the dogs' sex and size. This episodic-like memory decline observed in elderly dogs may be related to the physiological process of aging or preclinical pathological manifestation of cognitive impairment, similar as reported in humans. More studies should be carried out evaluating episodic-like memory in dogs with suspected of canine cognitive dysfunction syndrome in order to better understand the physiological and pathological behavior of this type of memory in canine species.
... Evidence for mental time travel into the past, based on the acquisition of space-time-content associations in one-trial or multiple learning trials (see [51] for a critique of multiple-learning trials), has been found in several different species. Great apes [110], dogs [67], cats [144], mice [49], rats [93], birds [28,160], zebrafish [80], cuttlefish [89], and insects [125] were all reported to have the ability to mentally travel though time. ...
Article
The evolution of intellectual capacities has brought forth a continuum of consciousness levels subserved by neuronal networks of varying complexity. Brain pathologies, neurodegenerative, and mental diseases affect conscious cognition and behavior. Although impairments in consciousness are among the most devastating consequences of neurological and mental diseases, valid and reliable animal models of consciousness, that could be used for preclinical research are missing. The platform theory holds that the brain enters a conscious operation mode, whenever mental representations of stimuli, associations, concepts, memories, and experiences are effortfully maintained (in working memory) and actively manipulated. We used the platform theory as a framework and evaluation standard to categorize behavioral paradigms with respect to the level of consciousness involved in task performance. According to the platform theory, a behavioral paradigm involves conscious cognitive operations, when the problem posed is unexpected, novel or requires the maintenance and manipulation of a large amount of information to perform cognitive operations on them. Conscious cognitive operations are associated with a relocation of processing resources and the redirection of attentional focus. A consciousness behavioral test battery is proposed that is composed of tests which are assumed to require higher levels of consciousness as compared to other tasks and paradigms. The consciousness test battery for rodents includes the following tests: Working memory in the radial arm maze, episodic-like memory, prospective memory, detour test, and operant conditioning with concurrent variable-interval variable-ratio schedules. Performance in this test battery can be contrasted with the performance in paradigms and tests that require lower levels of consciousness. Additionally, a second more comprehensive behavioral test battery is proposed to control for behavioral phenotypes not related to consciousness. We hope that the ideas presented here could serve as a guidance for the decryption of the neurobiological basis of consciousness.
... Both dogs and cats recognize depletion of food caused by their own actions. They can retrieve incidentally encoded information from a single past event in a foodexploration task, choosing the container from which they had not eaten food (dogs; Fujita et al. 2012, cats;Takagi et al. 2017). Macpherson and Roberts (2010) showed that dogs in radial maze tests easily learned the "win-shift rule", avoiding locations where they previously consumed rewards. ...
Article
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Dogs and cats are sensitive to human social signals such as pointing, gazing and facial expressions. Previous studies have demonstrated that dogs show over-reliance on human actions in the presence of conflicting physical cues. However, it is still unclear whether this tendency is specific to dogs, or shared with other domesticated animals. Here, we compared the behavior of dogs and cats in a two-choice task after they saw a person taking and pretending to eat food from a baited container. After one experimenter showed the dogs (Experiment 1) or cats (Experiment 2) two opaque containers, each containing a piece of the food, another (the demonstrator) removed food from one container and ate it (Eating condition), or simply picked up the food and returned it to the container (Showing condition). We recorded which container the subjects approached first after the demonstration. Both dogs and cats were less likely to choose the container associated with the human in the Eating than the Showing condition, although choice for this container was above chance in both conditions. In Experiment 3, we confirmed that dogs and cats naturally chose a baited over an empty container. These results suggest that both species’ reasoning abilities might be influenced by a bias for prioritizing specific human actions. Although dogs and cats have different domestication histories, their social awareness of humans appears similar, possibly because they both share their environment with humans.
... In the case of cats (Takagi et al., 2017), we adopted almost the same procedure as the one used with dogs, except that instead of using a leash, the owners controlled their cat's behavior by direct handling. Results showed that, like dogs, cats preferentially explored the feeder they had not eaten from, suggesting that they also used the incidentally encoded memory of their (non-)feeding experience. ...
Article
Humans have mental time in our mind, apart from physical time that is a part of system that governs the physical world, and memory is our key cognitive ability for recognizing the passage of time. Recent studies have suggested that the memory system of several nonhuman animals may have an incidental nature, which is also a feature of episodic memory. In addition, apes, which are phylogenetically close to humans, have an ability to remember a single past event. In the case of humans, preverbal infants under the age of two are able to retain long-term memory of a single event and apply it to predict a future event. Thus, nonhuman animals and preverbal human infants both have their own specific mental time travel abilities, and there is a phylogenetic and ontogenic basis of full-fledged mental time travel that can be found in human adults.
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Episodic-like memory in non-human animals represents the behavioral characteristics of human episodic memory—the ability to mentally travel backward in time to “re-live” past experiences. A focus on traditional model species of episodic-like memory may overlook taxa possessing this cognitive ability and consequently its evolution across species. Experiments conducted in the wild have the potential to broaden the scope of episodic-like memory research under the natural conditions in which they evolved. We combine two distinct yet complementary episodic-like memory tasks (the what-where-when memory and incidental encoding paradigms), each targeting a different aspect of human episodic memory, namely the content (what-where-when) and process (incidental encoding), to comprehensively test the memory abilities of wild, free-living, non-caching blue tits (Cyanistes caeruleus) and great tits (Parus major). Automated feeders with custom-built programs allowed for experimental manipulation of spatiotemporal experiences on an individual-level basis. In the what-where-when memory experiment, after learning individualized temporal feeder rules, the birds demonstrated their ability to recall the “what” (food type), “where” (feeder location), and “when” (time since their initial visit of the day) of previous foraging experiences. In the incidental encoding experiment, the birds showed that they were able to encode and recall incidental spatial information regarding previous foraging experiences (“where” test), and juveniles, but not adults, were also able to recall incidentally encoded visual information (“which” test). Consequently, this study presents multiple lines of converging evidence for episodic-like memory in a wild population of generalist foragers, suggesting that episodic-like memory may be more taxonomically widespread than previously assumed.
Article
The affordance of an object refers to its functional properties. For example, a bowl has the affordance of holding water, but a sieve does not. Here, we report that ants learn the affordance of a novel object without this attribute being rewarded, and use the memory of this affordance to avoid predicted, but never experienced, crowding. Ants were trained to feeders, which could support either only one ant or many. Two feeders were encountered, each of identical design but differently scented. After training, on the outward journey, half the ants encounter nestmates, which had fed on food matching one of the training feeders. Encountering returning nestmates reduced preference for the feeder matching the scent of the encountered nestmates, but only for ants trained on a limited-access feeder; ants trained on an unlimited feeder were unaffected. In other words, only if ants know that the food access is limited, and receive information that this feeder is heavily visited, do they reduce their preference for this feeder. To achieve this, the ants had to combine memories of the feeders' affordance with the presence of nestmates. Then they had to use semantic knowledge that restricted food access combined with nestmate presence predicts a likelihood of crowding, or a rule such as "if the food is restricted and there are nestmates on the path, go to another food source." Regardless of the mechanism, these results demonstrate that ants latently learn the affordance of their surroundings, an unexpected cognitive ability for an invertebrate.
Article
Practical relevance The ‘2022 ISFM/AAFP Cat Friendly Veterinary Environment Guidelines’ (hereafter the ‘Cat Friendly Veterinary Environment Guidelines’) describe how the veterinary clinic environment can be manipulated to minimise feline patient distress. Many components of a veterinary clinic visit or stay may result in negative experiences for cats. However, much can be done to improve a cat’s experience by making the veterinary clinic more cat friendly. Exposure to other cats and other species can be reduced, and adjustments made with consideration of the feline senses and species-specific behaviour. Caregivers can prepare cats for a clinic visit with appropriate advice. Waiting rooms, examination rooms, hospital wards and other clinic areas can be designed and altered to reduce stress and hence encourage positive emotions. Changes need not be structural or expensive in order to be effective and make a difference to the cats and, in turn, to cat caregivers and the veterinary team. Moreover, by improving the all-round experience at the veterinary clinic, there are positive effects on preventive healthcare, identification of and recovery from illness, and compliance with treatment. Clinical challenges Good feline healthcare necessitates visiting the veterinary clinic, which, simply by being outside of a cat’s territory and familiar surroundings, may lead to negative experiences. Such experiences can trigger negative (protective) emotions and associated physiological stress, which can result in misleading clinical findings, patient distress, prolonged recovery from illness, further difficulties with handling at subsequent visits and potential veterinary personnel injury. There may be a mistaken belief that veterinary clinics must undergo significant renovation or building work to become cat friendly, and that, if species cannot be separated, then clinics cannot improve their care of cats. These Guidelines aim to dispel any such misconceptions and provide detailed practical advice. Evidence base These Guidelines have been created by a Task Force of experts convened by the International Society of Feline Medicine and American Association of Feline Practitioners, based on an extensive literature review and, where evidence is lacking, the authors’ experience. Endorsements: These Guidelines have been endorsed by a number of groups and organisations, as detailed on page 1161 and at icatcare.org/cat-friendly-guidelines and catvets.com/environment .
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The evolution of intellectual capacities has brought forth a continuum of consciousness levels subserved by neuronal networks of varying complexity. Brain pathologies, neurodegenerative, and mental diseases affect conscious cognition and behavior. Although impairments in consciousness are among the most devastating consequences of neurological and mental diseases, valid and reliable animal models of consciousness, that could be used for preclinical research are missing. The platform theory holds that the brain enters a conscious operation mode, whenever mental representations of stimuli, associations, concepts, memories, and experiences are effortfully maintained (in working memory) and actively manipulated. We used the platform theory as a framework and evaluation standard to categorize behavioral paradigms with respect to the level of consciousness involved in task performance. According to the platform theory, a behavioral paradigm involves conscious cognitive operations, when the problem posed is unexpected, novel or requires the maintenance and manipulation of a large amount of information to perform cognitive operations on them. Conscious cognitive operations are associated with a relocation of processing resources and the redirection of attentional focus. A consciousness behavioral test battery is proposed that is composed of tests which are assumed to require higher levels of consciousness as compared to other tasks and paradigms. The consciousness test battery for rodents includes the following tests: Working memory in the radial arm maze, episodic-like memory, prospective memory, detour test, and operant conditioning with concurrent variable-interval variable-ratio schedules. Performance in this test battery can be contrasted with the performance in paradigms and tests that require lower levels of consciousness. Additionally, a second more comprehensive behavioral test battery is proposed to control for behavioral phenotypes not related to consciousness. We hope that the ideas presented here could serve as a guidance for the decryption of the neurobiological basis of consciousness. Key words: Platform theory of consciousness, behavioral phenotyping, neural correlates of consciousness, composite score, disorders of consciousness, animal consciousness, behavioral test battery
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Cats, along with dogs, are one of the most popular companion animals for humans. Across the world, increasing numbers of cats are being kept as pets. Despite their familiarity, cats’ cognition has long been shrouded in mystery, mainly because cats were considered largely unsuitable for psychological studies in laboratory settings. The “Cats Team” in Kazuo Fujita’s lab has developed several innovative and useful methods for studying cat cognition. In this chapter, I review findings from some of the team’s studies of cat cognition, including physical inference, use human social cues, incidental memory, cross-modal integration, jealousy, and third-party social evaluation. I also briefly describe some ongoing work on the relation between genes and personality, and suggest directions in which behavioral and cognitive studies of cats might go.
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Humans spend the lion's share of their mental life either in their personal past or an anticipated or imagined future. This type of mental state is known as mental time travel. It is perhaps the most sophisticated and fitness-promoting cognition that has evolved in humans and with some reservation in animals. We have proposed that working memory capacity and the complexity of executive functions within working memory might limit the authenticity with which past events are reconstructed and anticipated or imagined future scenarios are constructed. In the present article, we discuss the possibility of a co-evolution between working memory capacity, complexity of executive functions available in the working memory workspace, and mental time travel abilities across species. We further assume that a complex working memory system can be constructed with quite different brains and conclude that the advanced cognitive function of thinking about the past and the future might not be a privilege of the mammalian brain.
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This article contains the argument that the human ability to travel mentally in time constitutes a discontinuity between ourselves and other animals. Mental time travel comprises the mental reconstruction of personal events from the past (episodic memory) and the mental construction of possible events in the future. It is not an isolated module, but depends on the sophistication of other cognitive capacities, including self-awareness, meta-representation, mental attribution, understanding the perception-knowledge relationship, and the ability to dissociate imagined mental states from one's present mental state. These capacities are also important aspects of so-called theory of mind, and they appear to mature in children at around age 4. Furthermore, mental time travel is generative, involving the combination and recombination of familiar elements, and in this respect may have been a precursor to language. Current evidence, although indirect or based on anecdote rather than on systematic study, suggests that nonhuman animals, including the great apes, are confined to a "present" that is limited by their current drive states. In contrast, mental time travel by humans is relatively unconstrained and allows a more rapid and flexible adaptation to complex, changing environments than is afforded by instincts or conventional learning. Past and future events loom large in much of human thinking, giving rise to cultural, religious, and scientific concepts about origins, destiny, and time itself.
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The ability of domestic dogs (C. lupus famaliaris) to follow and attend to human emotion expressions is well documented. It is unknown whether domestic cats (F. silvestris catus) possess similar abilities. Because cats belong to the same order (Carnivora), but did not evolve to live in complex social groups, research with them enables us to tease apart the influence of social structure versus domestication processes on the capacity to recognize human communicative cues, such as emotions. Two experiments were conducted to determine the extent to which domestic cats discriminate between human emotion cues. The first experiment presented cats with facial and postural cues of happiness and anger from both an unfamiliar experimenter and their familiar owner in the absence of vocal cues. The second experiment presented cats with vocal cues of human emotion through a positively or negatively charged conversation between an experimenter and owner. Domestic cats were only modestly sensitive to emotion, particularly when displayed by their owner, suggesting that a history of human interaction alone may not be sufficient to shape such abilities in domestic cats.
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Cats’ (Felis catus) communicative behaviour towards humans was explored using a social referencing paradigm in the presence of a potentially frightening object. One group of cats observed their owner delivering a positive emotional message, whereas another group received a negative emotional message. The aim was to evaluate whether cats use the emotional information provided by their owners about a novel/unfamiliar object to guide their own behaviour towards it. We assessed the presence of social referencing, in terms of referential looking towards the owner (defined as looking to the owner immediately before or after looking at the object), the behavioural regulation based on the owner’s emotional (positive vs negative) message (vocal and facial), and the observational conditioning following the owner’s actions towards the object. Most cats (79 %) exhibited referential looking between the owner and the object, and also to some extent changed their behaviour in line with the emotional message given by the owner. Results are discussed in relation to social referencing in other species (dogs in particular) and cats’ social organization and domestication history.
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Many recent comparative studies have addressed "episodic" memory in nonhuman animals, suggesting that birds, rodents, great apes, and others can remember their own behavior after at least a half-day delay. By contrast, despite numerous studies regarding long-term memory, few comparable studies have been conducted on short-term retention for own behavior. In the current study, we addressed the following question: Do chimpanzees remember what they have just done? Four chimpanzees performed matching-to-sample and visual search tasks on a routine basis and were occasionally (every four sessions) given a "recognition" test immediately after their response during visual search trials. Even though these test trials were given very rarely, all four chimpanzees chose the stimulus they selected in the visual search trials immediately before the test trial significantly more frequently than they chose the stimulus they selected in another distractor trial. Subsequent experiments ruled out the possibility that preferences for the specific stimuli accounted for the recognition test results. Thus, chimpanzees remembered their own behavior even within a short-term interval. This type of memory may involve the transfer of episodic information from working memory to long-term episodic-like memory (i.e., an episodic buffer).
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Dogs have been shown to discriminate between human facial expressions, and they seem to use human emotional communication to regulate their behaviour towards an external object/situation. However, it is still not clear (1) whether they just respond to the emotional message received with a corresponding increase/decrease in their level of activation or whether they perceive that the emotional message refers to a specific object, (2) which emotional message they use to modify their behaviour (i.e. whether they are following the positive message or avoiding the negative one) and (3) whether their familiarity with the informant has an effect on the dogs' behaviour. To address these issues, five groups of dogs were tested in two experiments. The first group observed the owner delivering two different emotional messages (happiness and fear) towards two identical objects hidden behind barriers, and the second group observed the owner delivering the same emotional messages but with no-objects present in the room. The third and the fourth groups observed the owner delivering a happy versus a neutral, and a negative versus a neutral emotional message towards the hidden objects. Finally, the fifth group observed a stranger acting like the owner of the first group. When the owner was acting as the informant, dogs seemed to be capable of distinguishing between a fearful and happy emotional expression and preferentially chose to investigate a box eliciting an expression of happiness rather than of fear or neutrality. Dogs, however, seemed to have greater difficulty in distinguishing between the fearful and neutral emotional messages delivered by the owner and between the happy and fearful expressions delivered by the stranger. Results suggest that dogs have learned to associate their owners' positive emotional messages to positive outcomes, and hence use their communicative messages to guide their actions. However, negative emotional messages and those delivered by strangers are not as clear to dogs.
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Examined the ability of Sprague-Dawley rats to follow different food-searching strategies in a test of spatial memory. In a win–shift procedure, Ss were rewarded for choosing locations different from ones just chosen and in a win–stay procedure, they were rewarded for returning to the locations just chosen. In a 3rd procedure, Ss were rewarded for every choice. The win–shift strategy was learned rapidly and was performed well, whereas the win–stay strategy was learned slowly, if at all. When every choice was rewarded, Ss exhibited a preference for following a win–shift strategy. Data indicate that rats are disposed to follow a win–shift strategy when searching for food. First, they are able to learn a win–shift procedure better than they are able to learn a win–stay procedure. Second, when any choice produces reward, they prefer to follow a win–shift strategy. The influence of this win–shift disposition on food gathering in the wild and on performance of laboratory discrimination tasks is discussed. (25 ref) (PsycINFO Database Record (c) 2012 APA, all rights reserved)
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Social referencing is a process whereby an individual uses the emotional information provided by an informant about a novel object/stimulus to guide his/her own future behaviour towards it. In this study adult dogs were tested in a social referencing paradigm involving a potentially scary object with either their owner or a stranger acting as the informant and delivering either a positive or negative emotional message. The aim was to evaluate the influence of the informant's identity on the dogs' referential looking behaviour and behavioural regulation when the message was delivered using only vocal and facial emotional expressions. Results show that most dogs looked referentially at the informant, regardless of his/her identity. Furthermore, when the owner acted as the informant dogs that received a positive emotional message changed their behaviour, looking at him/her more often and spending more time approaching the object and close to it; conversely, dogs that were given a negative message took longer to approach the object and to interact with it. Fewer differences in the dog's behaviour emerged when the informant was the stranger, suggesting that the dog-informant relationship may influence the dog's behavioural regulation. Results are discussed in relation to studies on human-dog communication, attachment, mood modification and joint attention.
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Little is known about how animals represent their own actions in working memory. We investigated whether bottlenosed dolphins could recall actions they had recently performed and reveal those recollections using an abstract rule. Two dolphins were trained to respond to a specific gestural command by repeating the last behavior performed. Both dolphins proved to be able to repeat a wide variety of behaviors on command and were able to generalize the repeating rule to novel behaviors and situations. One dolphin was able to repeat all 36 behaviors she was tested on, including behaviors involving multiple simultaneous actions and self-selected behaviors. These results suggest that dolphins can flexibly access memories of their recent actions and that these memories are of sufficient detail to allow for reenactments. The repeating task can potentially be used to investigate short-term action and event representations in a variety of species.
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Social referencing is the seeking of information from another individual to form one's own understanding and guide action. In this study, adult dogs were tested in a social referencing paradigm involving their owner and a potentially scary object. Dogs received either a positive or negative message from the owner. The aim was to evaluate the presence of referential looking to the owner, behavioural regulation based on the owner's (vocal and facial) emotional message and observational conditioning following the owner's actions towards the object. Most dogs (83%) looked referentially to the owner after looking at the strange object, thus they appear to seek information about the environment from the human, but little differences were found between dogs in the positive and negative groups as regards behavioural regulation: possible explanations for this are discussed. Finally, a strong effect of observational conditioning was found with dogs in the positive group moving closer to the fan and dogs in the negative group moving away, both mirroring their owner's behaviour. Results are discussed in relation to studies on human-dog communication, attachment and social learning.
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Episodic memory, as defined by Tulving, can be described in terms of behavioural elements (what, where and when information) but it is also accompanied by an awareness of one's past (chronesthesia) and a subjective conscious experience (autonoetic awareness). Recent experiments have shown that corvids and rodents recall the where, what and when of an event. This capability has been called episodic-like memory because it only fulfils the behavioural criteria for episodic memory. We tested seven chimpanzees, three orangutans and two bonobos of various ages by adapting two paradigms, originally developed by Clayton and colleagues to test scrub jays. In Experiment 1, subjects were fed preferred but perishable food (frozen juice) and less preferred but non-perishable food (grape). After the food items were hidden, subjects could choose one of them either after 5 min or 1 h. The frozen juice was still available after 5 min but melted after 1 h and became unobtainable. Apes chose the frozen juice significantly more after 5 min and the grape after 1 h. In Experiment 2, subjects faced two baiting events happening at different times, yet they formed an integrated memory for the location and time of the baiting event for particular food items. We also included a memory task that required no temporal encoding. Our results showed that apes remember in an integrated fashion what, where and when (i.e., how long ago) an event happened; that is, apes distinguished between different events in which the same food items were hidden in different places at different times. The temporal control of their choices was not dependent on the familiarity of the platforms where the food was hidden. Chimpanzees' and bonobos' performance in the temporal encoding task was age-dependent, following an inverted U-shaped distribution. The age had no effect on the performance of the subjects in the task that required no temporal encoding.
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The present study examined working memory for what, where, and when information in rhesus monkeys (Macaca mulatta) using a computerized task. In Experiment 1, monkeys completed three delayed matching-to-sample (DMTS) tasks: (1) identity DMTS, (2) spatial DMTS, and (3) temporal DMTS. In Experiment 2, the identity and spatial tasks were combined so that monkeys had to report both what and where information about an event. In Experiment 3, the identity, spatial, and temporal tasks were combined to examine what-where-when memory integration. The rhesus monkeys reported all three components of the events, and there was some evidence suggesting that these components were integrated in working memory.
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Some animals have been shown to be able to remember which type of food they hoarded or encountered in which location and how long ago (what-where-when memory). In this study, we test whether magpies (Pica pica) also show evidence of remembering these different aspects of a past episode. Magpies hid red- and blue-dyed pellets of scrambled eggs in a large tray containing wood shavings. They were allowed to make as many caches as they wanted. The birds were then returned either the same day or the next day to retrieve the pellets. If they returned the same day, one colour of pellets was replaced with wooden beads of similar size and colour, while if they returned the next day this would happen to the other colour. Over just a few trials, the birds learned to only search for the food pellets, and ignore the beads, of the appropriate colour for the given retention interval. A probe trial in which all items were removed showed that the birds persisted in searching for the pellets and not the beads. This shows that magpies can remember which food item they hoarded where, and when, even if the food items only differ from each other in their colour and are dispersed throughout a continuous caching substrate.
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It has been proposed that memory for personal experiences (episodic memory, rather than semantic memory) relies on the conscious review of past experience and thus is unique to humans. In an attempt to demonstrate episodic-like memory in animals, we first trained pigeons to respond to the (nonverbal) question "Did you just peck or did you just refrain from pecking?" by training them on a symbolic matching task with differential responding required to the two line-orientation samples and reinforcing the choice of a red comparison if they had pecked and the choice of a green comparison if they had not pecked. Then, in Experiment 1, after providing the conditions for (but not requiring) the pigeons to peck at one new stimulus (a yellow hue) but not at another (a blue hue), we tested them with the new hue stimuli and the red and green comparisons. In Experiment 2, we tested the pigeons with novel stimuli (a circle, which they spontaneously pecked, and a dark response key, which they did not peck) and the red and green comparisons. In both experiments, pigeons chose the comparison appropriate to the response made to the test stimulus. Thus, the pigeons demonstrated that they could remember specific details about their past experiences, a result consistent with the notion that they have the capacity for forming episodic-like memories.
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Dogs' (Canis familiaris) and cats' (Felis catus) interspecific communicative behavior toward humans was investigated. In Experiment 1, the ability of dogs and cats to use human pointing gestures in an object-choice task was compared using 4 types of pointing cues differing in distance between the signaled object and the end of the fingertip and in visibility duration of the given signal. Using these gestures, both dogs and cats were able to find the hidden food; there was no significant difference in their performance. In Experiment 2, the hidden food was made inaccessible to the subjects to determine whether they could indicate the place of the hidden food to a naive owner. Cats lacked some components of attention-getting behavior compared with dogs. The results suggest that individual familiarization with pointing gestures ensures high-level performance in the presence of such gestures; however, species-specific differences could cause differences in signaling toward the human.
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This study explored the duration of cats' working memory for hidden objects. Twenty-four cats were equally divided into four groups, which differed according to the type of visual cues displayed on and/or around the hiding boxes. During eight sessions, the four groups of cats were trained to locate a desirable object hidden behind one of the four boxes placed in front of them. Then, the cats were tested with retention intervals of 0, 10, 30 and 60 s. Results revealed no significant differences between the groups during training or testing. In testing, the cats' accuracy to locate the hidden object rapidly declined between 0 and 30 s but remained higher than chance with delays of up to 60 s. The analysis of errors also indicated that the cats searched as a function of the proximity of the target box and were not subjected to intertrial proactive interference. This experiment reveals that the duration of cats' working memory for disappearing objects is limited and the visual cues displayed on and/or around the boxes do not help the cats to memorize a hiding position. In discussion, we explore why the duration of cats' working memory for disappearing objects rapidly declined and compare these finding with those from domestic dogs. The irrelevance of visual cues displayed on and around the hiding boxes on cats' retention capacity is also discussed.
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Some non-human animals may possess the ability to recall the "what", "where", and "when" of a single past event. We tested the hypothesis that male meadow voles possess the capacity to recall the "what", "where", and "when" of a single past event associated with mate selection in two experiments. Briefly, male voles were allowed to explore an apparatus that contained two chambers. One chamber contained a day-20 pregnant female (24 h prepartum). The other chamber contained a sexually mature female that was neither pregnant nor lactating (REF female). Twenty-four hour after the exposure, the males were placed in the same apparatus, which was empty and clean. At this time, the pregnant female would have entered postpartum estrus (PPE), a period of heightened sexual receptivity. Males initially chose and spent significantly more time investigating the chamber that originally housed the pregnant female (now a PPE female) than the chamber that originally housed the REF female. Male voles also explored an apparatus containing a chamber with a PPE female and one chamber containing a REF female. Twenty-four hour later, males were placed into an empty and clean apparatus. The males did not display an initial choice and they spent similar amounts of time investigating the chamber that originally housed the PPE female (now a lactating female) and the chamber that originally housed the REF female. The results of these and additional experiments suggest that male voles may have the capacity to recall the "what", "where", and "when" of a single past event, which may allow males to remember the location of females who would currently be in heightened states of sexual receptivity.
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If pigeons are trained on matching-to-sample with differential responding required to the two samples, there is evidence that the differential responding can control comparison choice. We asked whether similar responding required at two different locations could also serve as the basis for comparison choice. Pigeons were pretrained to report the location that they had pecked. To reduce the likelihood that they could use the presence of differential proprioceptive cues at the time of their report, a common response was required between the location response and the comparison choice. They were then given experience with a conditional discrimination in which location of the comparison response varied randomly and was incidental to the choice of comparison. On test trials, after the pigeons had made their comparison choice, they showed a significant tendency to choose the appropriate test comparison when they were unexpectedly asked to report the location of their previous pecking response. These results have implications for the demonstration of episodic-like memory in pigeons because they suggest that pigeons have the capacity to recall, unexpectedly, specific details about their past experiences.
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This study investigates how the colour, shape and location of patterns could be memorized within a time frame. Bees were trained to visit two Y-mazes, one of which presented yellow vertical (rewarded) versus horizontal (non-rewarded) gratings at one site in the morning, while another presented blue horizontal (rewarded) versus vertical (non-rewarded) gratings at another site in the afternoon. The bees could perform well in the learning tests and various transfer tests, in which (i) all contextual cues from the learning test were present; (ii) the colour cues of the visual patterns were removed, but the location cue, the orientation of the visual patterns and the temporal cue still existed; (iii) the location cue was removed, but other contextual cues, i.e. the colour and orientation of the visual patterns and the temporal cue still existed; (iv) the location cue and the orientation cue of the visual patterns were removed, but the colour cue and temporal cue still existed; (v) the location cue, and the colour cue of the visual patterns were removed, but the orientation cue and the temporal cue still existed. The results reveal that the honeybee can recall the memory of the correct visual patterns by using spatial and/or temporal information. The relative importance of different contextual cues is compared and discussed. The bees' ability to integrate elements of circadian time, place and visual stimuli is akin to episodic-like memory; we have therefore named this kind of memory circadian timed episodic-like memory.
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The chapter tackles the placement of self-reflective consciousness amongst the numberless gradations by Darwin. Discussions of self-consciousness inevitably lead to Descartes' dictum, "I think, therefore I am". The goal is a rapprochement between this view and the Cartesian view, emphasizing this kind of consciousness applicable only to humans. Descartes maintained that animals are unable to engage in self-reflection. Negative results of various ape language projects and broad advances in animal cognition suggest that Descartes was right about the uniqueness of language but that he was wrong about animal's capacity for thought and self-reflection. There is abundant evidence that nonhuman pirates can form representations and use them to solve problems. The concept of autonoetic consciousness, as Tulving calls it, seemed close to the construct of self-reflective consciousness and metacognition which was the concern. Thus, instead of focusing on language, more fundamental capabilities are considered-the origins of self-reflective consciousness.
Article
The recollection of past experiences allows us to recall what happened during a particular event, and where and when it occurred [1]. Since the first study on episodic-like memory in scrub-jays [2], there has been widespread acceptance of the idea that tests in animals should integrate the 'what', 'where' and 'when' components of a unique event that occurred in the past [3,4]. This is referred to as episodic-like memory rather than episodic memory per se, in acknowledgement of the lack of evidence for, or against, the phenomenological aspects that accompany episodic recollection in humans. So far, evidence for episodic-like memory has only been found in some birds and mammals. We show here that cuttlefish, cephalopod mollusks, keep track of what they have eaten, and where and how long ago they ate, in order to match their foraging behavior with the time of replenishing of different foods. Foraging in cuttlefish fulfils the criteria of 'what', 'where' and 'when' of unique events and thus provides behavioral evidence of episodic-like memory in an invertebrate.
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Memory processing in nonhuman animals has been typically tested in situations where the animals are repeatedly trained to retrieve their memory trace, such as delayed matching to sample, serial probe recognition, etc. In contrast, how they utilize incidentally formed memory traces is not well investigated except in rodents. We examined whether domestic dogs could solve an unexpected test based on a single past experience. In Experiment 1, leashed dogs were led to 4 open, baited containers and allowed to eat from 2 of them (Exposure phase). After a walk outside for more than 10 min, during which time the containers were replaced with new identical ones, the dogs were unexpectedly returned to the site and unleashed for free exploration (test phase). Eleven out of 12 dogs first visited one of the containers from which they had not eaten. In Experiment 2, two containers had food in them, one had a nonedible object, and the last one was empty. Dogs visited all 4 containers and were allowed to eat one of the food rewards in the Exposure phase. In the test phase, unleashed dogs first visited the previously baited container from which they had not eaten significantly more often than chance. These results demonstrate that in an unexpected, test dogs may retrieve "what" and "where" information about seen (now invisible) items from incidental memory formed during a single past experience.
Article
A fundamental aspect of episodic memory is that retrieval of information can occur when encoding is incidental and memory assessment is unexpected. These features are difficult to model in animals because behavioral training likely gives rise to well-learned expectations about the sequence of events. Thus, the possibility remains that animals may solve an episodic memory test by using well-learned semantic rules without remembering the episode at memory assessment. Here we show that rats can answer an unexpected question after incidental encoding in a hippocampal-dependent manner, consistent with the use of episodic memory. Rats were initially trained to report about a recent event (food versus no food) and separately searched for food where there was no expectation of being asked about the presence of food. To test episodic memory, we gave rats the opportunity to incidentally encode the presence or absence of food and unexpectedly asked them to report about the recent event. Temporary inactivation of the CA3 region of the hippocampus with bilateral infusions of lidocaine selectively eliminated the ability of rats to answer the unexpected, but not the expected, question. Our studies suggest that rats remember an earlier episode after incidental encoding based upon hippocampal-dependent episodic memory.
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The ability to recall features of environments not present to the senses is important in human thinking, planning, and communication, but to date there are almost no data on recall capabilities in nonverbal animals. In this study, the author used symbol knowledge as a tool to study chimpanzee memory. An 11-year-old female chimpanzee (Pan troglodytes) that had already learned a large number of arbitrarily designated geometric forms (lexigrams) watched as an experimenter hid an object in the woods outside her outdoor enclosure. The type and location of the object varied across trials. After an imposed delay of up to 16 h, the chimpanzee could interact indoors with a person who did not know that an object had been hidden, let alone the type or location of the object. A keyboard in the indoor cage displayed 256 lexigrams. From Trial 1, the chimpanzee seemed to do whatever it took to catch the person's attention and then touched the lexigram corresponding to the type of object hidden, pointed outdoors, went outdoors (if followed), and continued to point manually toward the object and vocalize until the person found the object. The subject indicated nonfood objects as well as more than 20 food types.
Article
Episodic memory is the ability to remember personally experienced past events (Tulving in Organization of memory. Academic Press, San Diego, pp. 381-403, 1972). In non-human animals, the behavioural criterion for episodic-like memory is remembering "what" occurred in conjunction with "when" and "where" (Clayton and Dickinson in Nature 395:272-274, 1998). We conducted tests for "what, where, and when" memory in a food-storing bird, the black-capped chickadee (Poecile atricapillus). In Experiment 1, chickadees found sunflower seeds and mealworms in concealed sites in their home cage. Birds later re-visited these sites after either a short (3 h) or long (123 h) retention interval. Chickadees normally prefer mealworms, but at the long retention interval mealworms were degraded in taste and appearance. Chickadees showed some memory for what kind of food they had encountered and where, but no memory for when food had previously been found. Experiment 2 followed a similar procedure, except that chickadees searched for hidden sunflower seeds and mealworms in trees in an indoor aviary. These more natural conditions increased both the spatial scale of the task and the effort required to find food. In this experiment, birds showed evidence for all three components of what-where-when memory. Unlike some previous studies of episodic-like memory, birds' behaviour cannot be accounted for by differential memory strength for more recent events. The results show that memory for what, where, and when occurs in food-storing birds outside the corvid family, does not require food caching or retrieval, and that remembering "when" can depend on the nature of the task.
Article
The recollection of past experiences allows us to recall what a particular event was, and where and when it occurred, a form of memory that is thought to be unique to humans. It is known, however, that food-storing birds remember the spatial location and contents of their caches. Furthermore, food-storing animals adapt their caching and recovery strategies to the perishability of food stores, which suggests that they are sensitive to temporal factors. Here we show that scrub jays (Aphelocoma coerulescens) remember 'when' food items are stored by allowing them to recover perishable 'wax worms' (wax-moth larvae) and non-perishable peanuts which they had previously cached in visuospatially distinct sites. Jays searched preferentially for fresh wax worms, their favoured food, when allowed to recover them shortly after caching. However, they rapidly learned to avoid searching for worms after a longer interval during which the worms had decayed. The recovery preference of jays demonstrates memory of where and when particular food items were cached, thereby fulfilling the behavioural criteria for episodic-like memory in non-human animals.
Article
[Figure: see text] ▪ Abstract Episodic memory is a neurocognitive (brain/mind) system, uniquely different from other memory systems, that enables human beings to remember past experiences. The notion of episodic memory was first proposed some 30 years ago. At that time it was defined in terms of materials and tasks. It was subsequently refined and elaborated in terms of ideas such as self, subjective time, and autonoetic consciousness. This chapter provides a brief history of the concept of episodic memory, describes how it has changed (indeed greatly changed) since its inception, considers criticisms of it, and then discusses supporting evidence provided by (a) neuropsychological studies of patterns of memory impairment caused by brain damage, and (b) functional neuroimaging studies of patterns of brain activity of normal subjects engaged in various memory tasks. I also suggest that episodic memory is a true, even if as yet generally unappreciated, marvel of nature.
Article
Episodic memory refers to the conscious recollection of a unique past experience in terms of "what" happened and "where" and "when" it happened. Since deficits in episodic memory are found in a number of neuropsychiatric diseases, such as Alzheimer's disease, for which several pharmacological, lesion and genetic animal models are available, there is a need for animal models of episodic-like memory, which can be used to devise appropriate treatments. However, even when the problem of conscious recollection in animals is factored out, episodic memory has been difficult to demonstrate in nonhuman mammals because it has not yet been possible to demonstrate an integrated memory for "what",-"where"-and-"when". We designed a three-trial "what",-"where"-and-"when" object exploration task in which different versions of the novelty preference paradigm were combined to subsume (a) object recognition memory, (b) the memory for locations in which objects were explored and (c) the temporal order memory for objects presented at distinct time points. Our results suggest that mice are able to (a) recognize previously explored objects, (b) remember the location in which particular objects were previously encountered and (c) discriminate the relative recency in which different objects were presented. We suggest that our protocol providing the simultaneous assessment of object memory for "what",-"where"-and-"when" in mice might be useful in the search for the neural substrates of episodic memory, the screening for promnestic drugs and the behavioral phenotyping of genetic models of neuropsychiatric diseases affecting episodic memory.
Article
A fundamental question in comparative cognition is whether animals remember unique, personal past experiences. It has long been argued that memories for specific events (referred to as episodic memory) are unique to humans. Recently, considerable evidence has accumulated to show that food-storing birds possess critical behavioral elements of episodic memory, referred to as episodic-like memory in acknowledgment of the fact that behavioral criteria do not assess subjective experiences. Here we show that rats have a detailed representation of remembered events and meet behavioral criteria for episodic-like memory. We provided rats with access to locations baited with distinctive (e.g., grape and raspberry) or nondistinctive (regular chow) flavors. Locations with a distinctive flavor replenished after a long but not a short delay, and locations with the nondistinctive flavor never replenished. One distinctive flavor was devalued after encoding its location by prefeeding that flavor (satiation) or by pairing it with lithium chloride (acquired taste aversion), while the other distinctive flavor was not devalued. The rats selectively decreased revisits to the devalued distinctive flavor but not to the nondevalued distinctive flavor. The present studies demonstrate that rats selectively encode the content of episodic-like memories.
Article
In a dynamic world, mechanisms allowing prediction of future situations can provide a selective advantage. We suggest that memory systems differ in the degree of flexibility they offer for anticipatory behavior and put forward a corresponding taxonomy of prospection. The adaptive advantage of any memory system can only lie in what it contributes for future survival. The most flexible is episodic memory, which we suggest is part of a more general faculty of mental time travel that allows us not only to go back in time, but also to foresee, plan, and shape virtually any specific future event. We review comparative studies and find that, in spite of increased research in the area, there is as yet no convincing evidence for mental time travel in nonhuman animals. We submit that mental time travel is not an encapsulated cognitive system, but instead comprises several subsidiary mechanisms. A theater metaphor serves as an analogy for the kind of mechanisms required for effective mental time travel. We propose that future research should consider these mechanisms in addition to direct evidence of future-directed action. We maintain that the emergence of mental time travel in evolution was a crucial step towards our current success.
Article
Recent experiments with rats suggest that they show episodic-like or what-where-when memory for a preferred food found on a radial maze. Although memory for when a salient event occurred suggests that rats can mentally travel in time to a moment in the past, an alternative possibility is that they remember how long ago the food was found. Three groups of rats were tested for memory of previously encountered food. The different groups could use only the cues of when, how long ago, or when + how long ago. Only the cue of how long ago food was encountered was used successfully. These results suggest that episodic-like memory in rats is qualitatively different from human episodic memory.
Episodic memory and autonoesis: uniquely human? The Missing Link in Cognition: Origins of Self-reflective Consciousness
  • E Tulving
Tulving, E., 2005. Episodic memory and autonoesis: uniquely human? In: Terrace, H.S., Metcalfe, J. (Eds.), The Missing Link in Cognition: Origins of Self-reflective Consciousness. Oxford University Press, pp. 3–56.
  • S Takagi
S. Takagi et al. / Behavioural Processes xxx (2016) xxx-xxx