Memory In Dogs Research Articles

Spatial working memory in a disappearing object task is impaired in female but not male dogs with chronic osteoarthritis

Chronic pain in humans is associated with impaired working memory but it is not known whether this is the case in long-lived companion animals, such as dogs, who are especially vulnerable to developing age-related chronic pain conditions. Pain-related impairment of cognitive function could have detrimental effects on an animal’s ability to engage with its owners and environment or to respond to training or novel situations, which may in turn affect its quality of life. This study compared the performance of 20 dogs with chronic pain from osteoarthritis and 21 healthy control dogs in a disappearing object task of spatial working memory. Female neutered osteoarthritic dogs, but not male neutered osteoarthritic dogs, were found to have lower predicted probabilities of successfully performing the task compared to control dogs of the same sex. In addition, as memory retention interval in the task increased, osteoarthritic dogs showed a steeper decline in working memory performance than control dogs. This suggests that the effects of osteoarthritis, and potentially other pain-related conditions, on cognitive function are more clearly revealed in tasks that present a greater cognitive load. Our finding that chronic pain from osteoarthritis may be associated with impaired working memory in dogs parallels results from studies of human chronic pain disorders. That female dogs may be particularly prone to these effects warrants further investigation.

Effects of proactive interference on olfactory memory in dogs.

Proactive interference (PI) occurs when memories of past events or stimuli intrude in the present moment, causing working memory (WM) errors. These errors are often measured through WM tests such as matching-to-sample (MTS). When the repetition of individual stimuli increases, there is a greater chance of these intrusions, and thus there can be a decrease in accuracy in such tasks. In two experiments, we explored the nature of PI on dog working memory. First, we manipulated the size of the set of odors (2, 6, trial-unique) used to construct each session to maximize (2-odor set) and minimize (trial-unique) within-session proactive interference during an olfactory MTS task. Matching-to-sample accuracy decreased with greater PI. Second, we adapted procedures originally designed for pigeons and rhesus macaques to determine the locus of PI in dogs. To test for proactive interference, probe trials were inserted into MTS sessions where sample odors from earlier trials reappeared as incorrect comparisons. Incorrect responses on these probe trials indicated proactive interference. These probe tests were conducted with a 0-s or 20-s retention interval in separate sessions. We found that dogs performed worse on the matching task when the source of interference (odor stimulus) was from the immediately preceding trial compared with when they were from trials further back in the session but only for the 0-s retention interval. These results are compared with previous work examining the effects of proactive interference on working memory in other species.

Aging-related episodic-like memory decline in dogs

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.

The Elevator Effect: Spatial Learning and Memory in Dogs Confound Different Floors in Multilevel Environments, and Cues Closer to a Reward Prime over Cues More Distant to One

The Elevator Effect: Spatial Learning and Memory in Dogs Confound Different Floors in Multilevel Environments, and Cues Closer to a Reward Prime over Cues More Distant to One

Two assays of working memory in companion dogs: The holeboard and disappearing object tasks

Variation in executive function and age-related cognitive decline may underlie the emergence of behaviour and welfare problems in dogs. A better understanding of such links, and of dog cognition in general, will be facilitated by the development of cognitive tasks that can be readily implemented, including with publicly-owned dogs that are available for relatively short testing periods. Working memory is a key component of cognitive and executive function that is often measured using tests such as delayed-non-match-to-sample or radial-arm maze which require extensive training and testing. Here we successfully adapt the Holeboard Task to measure working and reference memory in dogs, and show that another test of working memory, the Disappearing Object Task, can be performed in a single day. Working memory (p = 0.002) and reference memory (p < 0.001) scores in a 16-hole Holeboard Task (four holes baited) increased across sessions, with reference memory scores falling steeply as expected when the configuration of baited buckets changed. In the Disappearing Object Task dogs were able to successfully locate an object displaced behind one of four visual barriers, and their ability to do this fell as the memory retention interval (0 s, 30 s, 60 s, 120 s, 240 s) between hiding and locating the object increased (p < 0.001). Holeboard and Disappearing Object working memory measures were not correlated, possibly due to differences in the motivational context and exact learning demands of the tasks. In summary we show that the Holeboard Task can be adapted for use in dogs and that the Disappearing Object Task can be implemented in a single day. The latter task may be particularly useful for working memory studies of dogs owned by the public where prolonged access is often infeasible, and the three-day Holeboard Task is faster to implement than other commonly used laboratory-based tasks.

Odour-Evoked Memory in Dogs: Do Odours Help to Retrieve Memories of Food Location?

Simple SummaryThe ability of odors to evoke past memories has been widely reported in humans. Although olfaction is generally considered as the most important sense in dogs, little is known about its relationship with memory in this species. To investigate this issue, we trained dogs to memorize the location of five rewards while a specific odor (i.e., vanilla) was dispersed in the environment. After 24 h delay, dogs were divided in three groups, which performed two trials of the same spatial task in different conditions. The first group received a control odor (i.e., apple) in the first trial and the vanilla odor in the second trial; vice versa, the second group was exposed to the vanilla odor in the first test and to the apple odor in the second one. The third group, instead, performed the tests with no odors. We found that the exposure to vanilla odor significantly improved dogs’ performance in the spatial task, suggesting that the odor aided dogs to recall specific and detailed memories originally formed in its presence. The ability of odors to spontaneously trigger specific memories has been widely demonstrated in humans. Although increasing evidence support the role of olfaction on dogs’ emotions and cognitive processes, very little research has been conducted on its relationship with memory in this species. The present study aimed at investigating the role of olfaction in the recall of detailed memories originally formed in the presence of a specific odor (i.e., vanilla). To test this, three groups of participants were trained with the same spatial learning task while a specific odor (i.e., vanilla) was dispersed in the testing room. Subjects were then divided in three experimental groups and after 24 h delay, they were presented with the same spatial task. The first group (Group 1) performed the task in the presence of a novel odor (i.e., control), whereas the second (Group 2) and the third group (Group 3) carried out the test in the presence of the vanilla odor and no odor (Group 3), respectively. After a brief delay, the test was presented again to the three groups of dogs: subjects of Group 1 were now tested in the presence of the vanilla odor, whereas the Group 2 was tested with the control odor. The Group 3 received no odor in both tests. A significant improvement of dogs’ performance was registered in the control-vanilla odors condition (Group 1), suggesting that the exposure to the odor presented at the encoding time would prompt the recall of spatial memories in dogs.

Recall of Others’ Actions after Incidental Encoding Reveals Episodic-like Memory in Dogs

The existence of episodic memory in non-human animals is a debated topic that has been investigated using different methodologies that reflect diverse theoretical approaches to its definition. A fundamental feature of episodic memory is recalling after incidental encoding, which can be assessed if the recall test is unexpected [1]. We used a modified version of the "Do as I Do" method [2], relying on dogs' ability to imitate human actions, to test whether dogs can rely on episodic memory when recalling others' actions from the past. Dogs were first trained to imitate human actions on command. Next, they were trained to perform a simple training exercise (lying down), irrespective of the previously demonstrated action. This way, we substituted their expectation to be required to imitate with the expectation to be required to lie down. We then tested whether dogs recalled the demonstrated actions by unexpectedly giving them the command to imitate, instead of lying down. Dogs were tested with a short (1min) and a long (1hr) retention interval. They were able to recall the demonstrated actions after both intervals; however, their performance declined more with time compared to conditions in which imitation was expected. These findings show that dogs recall past events as complex as human actions even if they do not expect the memory test, providing evidence for episodic-like memory. Dogs offer an ideal model to study episodic memory in non-human species, and this methodological approach allows investigating memory of complex, context-rich events. VIDEO ABSTRACT.

Identification of learning and memory genes in canine; promoter investigation and determining the selective pressure.

One of the important behaviors of dogs is trainability which is affected by learning and memory genes. These kinds of the genes have not yet been identified in dogs. In the current research, these genes were found in animal models by mining the biological data and scientific literatures. The proteins of these genes were obtained from the UniProt database in dogs and humans. Not all homologous proteins perform similar functions, thus comparison of these proteins was studied in terms of protein families, domains, biological processes, molecular functions, and cellular location of metabolic pathways in Interpro, KEGG, Quick Go and Psort databases. The results showed that some of these proteins have the same performance in the rat or mouse, dog, and human. It is anticipated that the protein of these genes may be effective in learning and memory in dogs. Then, the expression pattern of the recognized genes was investigated in the dog hippocampus using the existing information in the GEO profile. The results showed that BDNF, TAC1 and CCK genes are expressed in the dog hippocampus, therefore, these genes could be strong candidates associated with learning and memory in dogs. Subsequently, due to the importance of the promoter regions in gene function, this region was investigated in the above genes. Analysis of the promoter indicated that the HNF-4 site of BDNF gene and the transcription start site of CCK gene is exposed to methylation. Phylogenetic analysis of protein sequences of these genes showed high similarity in each of these three genes among the studied species. The dN/dS ratio for BDNF, TAC1 and CCK genes indicates a purifying selection during the evolution of the genes.

Deferred imitation and declarative memory in domestic dogs

This study demonstrates for the first time deferred imitation of novel actions in dogs (Canis familiaris) with retention intervals of 1.5min and memory of familiar actions with intervals ranging from 0.40 to 10min. Eight dogs were trained using the 'Do as I do' method to match their own behaviour to actions displayed by a human demonstrator. They were then trained to wait for a short interval to elapse before they were allowed to show the previously demonstrated action. The dogs were then tested for memory of the demonstrated behaviour in various conditions, also with the so-called two-action procedure and in a control condition without demonstration. Dogs were typically able to reproduce familiar actions after intervals as long as 10min, even if distracted by different activities during the retention interval and were able to match their behaviour to the demonstration of a novel action after a delay of 1min. In the two-action procedure, dogs were typically able to imitate the novel demonstrated behaviour after retention intervals of 1.5min. The ability to encode and recall an action after a delay implies that facilitative processes cannot exhaustively explain the observed behavioural similarity and that dogs' imitative abilities are rather based on an enduring mental representation of the demonstration. Furthermore, the ability to imitate a novel action after a delay without previous practice suggests presence of declarative memory in dogs.

Incidental memory in dogs: Adaptive behavioral solution at an unexpected memory test

Incidental memory in dogs: Adaptive behavioral solution at an unexpected memory test

Incidental memory in dogs (Canis familiaris): adaptive behavioral solution at an unexpected memory test

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 10min, 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.

The effect of frequency and duration of training sessions on acquisition and long-term memory in dogs

Most domestic dogs are subjected to some kind of obedience training, often on a frequent basis, but the question of how often and for how long a dog should be trained has not been fully investigated. Optimizing the training as much as possible is not only an advantage in the training of working dogs such as guide dogs and police dogs, also the training of family dogs can benefit from this knowledge. We studied the effect of frequency and duration of training sessions on acquisition and on long-term memory. Forty-four laboratory Beagles were divided into 4 groups and trained by means of operant conditioning and shaping to perform a traditional obedience task, each dog having a total of 18 training sessions. The training schedules of the 4 groups differentiated in frequency (1–2 times per week vs. daily) and duration (1 training session vs. 3 training sessions in a row). Acquisition was measured as achieved training level at a certain time. The dogs’ retention of the task was tested four weeks post-acquisition. Results demonstrated that dogs trained 1–2 times per week had significantly better acquisition than daily trained dogs, and that dogs trained only 1 session a day had significantly better acquisition than dogs trained 3 sessions in a row. The interaction between frequency and duration of training sessions was also significant, suggesting that the two affect acquisition differently depending on the combination of these. The combination of weekly training and one session resulted in the highest level of acquisition, whereas the combination of daily training and three sessions in a row resulted in the lowest level of acquisition. Daily training in one session produced similar results as weekly training combined with three sessions in a row. Training schedule did not affect retention of the learned task; all groups had a high level of retention after 4 weeks. The results of the study can be used to optimize training in dogs, which is important since the number of training sessions often is a limiting factor in practical dog training. The results also suggest that, once a task is learned, it is likely to be remembered for a period of at least four weeks after last practice, regardless of frequency and duration of the training sessions.

THE CANINE SAND MAZE: AN APPETITIVE SPATIAL MEMORY PARADIGM SENSITIVE TO AGE-RELATED CHANGE IN DOGS

Aged dogs exhibit a spectrum of cognitive abilities including a syndrome similar to Alzheimer's disease. A major impediment to research so far has been the lack of a quick and accurate test of visuospatial memory appropriate for community-based animals. We therefore report on the development and validation of the Canine Sand Maze. A 4.5-m-diameter circular pool was filled with a sand and powdered food reward mix to a depth of 10 cm. Dogs were given 4 habituation and 16 learning trials which alternated a food reward being half (control trials) or fully-buried (acquisition trials) in a fixed location. After a 90-min break, a probe trial was conducted. Cognitively normal, aged (> 8 years, n = 11) and young (1-4 years, n = 11), breed-matched dogs were compared. After correction for differences in control trials, average probe times were 2.97 and 10.81 s for young and aged dogs, respectively. In the probe trial, both groups spent significantly more time in the target quadrant but there was a trend for young dogs to cross a 1 m(2) annulus zone around the buried reward more frequently (2.6 times) than aged dogs (1.5 times). Test-retest reliability in a subset of young dogs (n = 5) was high. On the basis of these findings, the Canine Sand Maze is presented as a quick, sensitive and nonaversive tool for assessing spatial learning and reference memory in dogs.

Spatial memory in dogs (Canis familiaris) on a radial maze.

Working spatial memory in dogs (Canis familiaris) was tested in Experiments 1 and 2 on an 8-arm radial maze. When dogs chose freely among all 8 arms containing food in Experiment 1, they learned to enter all 8 arms with progressively fewer arm visits over trials. In Experiment 2, 2 groups of dogs were forced to visit 4 randomly chosen arms on the maze and then tested for memory of these arm visits using a win-shift rule for 1 group and a win-stay rule for the other group. Dogs performed better with the win-shift rule than with the win-stay rule. In Experiment 3, reference memory was investigated by using a 4-arm maze on which 0, 1, 3, and 6 pieces of food were consistently placed on different arms. Dogs learned to visit the arms with the larger amounts before the arms with the smaller amounts. Dogs' memory capacity in these studies was found to be surprisingly low.

Dose-specific effects of scopolamine on canine cognition: impairment of visuospatial memory, but not visuospatial discrimination.

The cholinergic system is linked extensively to memory, but its exact role remains controversial. In particular, scopolamine-induced impairment in rodents is not task specific, which may be due to difficulty in developing rodent protocols to assess deficits in recent memory, in which the remembered event is brief and distinct, and/or to non-specific behavioral impairment. The present study sought to determine whether scopolamine-induced deficits in recent memory, using a working memory task, could be dose-specifically dissociated from deficits in associative memory in dogs. A Latin-square design was used to determine the effect of scopolamine (5, 10 and 15 microg/kg; SC) on a variable delayed-non-matching-to-position (DNMP) task, which assesses visuospatial working memory. Subsequently, the minimal effective dose (15 microg/kg; SC) was administered prior to testing on a landmark discrimination task, which provides a measure of allocentric spatial ability, a black-white discrimination task, an oddity discrimination task and tests of exploratory behavior. We also investigated the effects of a 30 microg/kg dose (SC) on tests of oddity discrimination and behavioral activity. A 15 microg/kg dose produced significant impairment on the DNMP task, but did not affect performance of any discrimination task and did not alter behavior on tests of open field or curiosity. A 30 microg/kg dose caused disruption on discrimination performance and on open field measures. Working memory performance is most sensitive to scopolamine-induced impairment and can be dissociated from scopolamine-induced deficits in discrimination performance and non-cognitive behaviors. The present results indicate that scopolamine-induced impairments of working memory in the dog can serve as a model of age-related cholinergic dysfunction.

Neither perirhinal/entorhinal nor hippocampal lesions impair short-term auditory recognition memory in dogs

Visual, tactile, and olfactory recognition memory in animals is mediated in part by the perirhinal/entorhinal (or rhinal) cortices and, possibly, the hippocampus. To examine the role of these structures in auditory memory, we performed rhinal, hippocampal, and combined lesions in groups of dogs trained in auditory delayed matching-to-sample with trial-unique sounds. The sample sound was presented through a central speaker and, after a delay, the sample sound and a different sound were played alternately through speakers placed on either side of the animal; the animal was rewarded for responding to the side emitting the sample sound. None of the lesion groups showed significant impairment in comparison either to their own preoperative performance or to the performance of intact control dogs. This was the case both for relearning the delayed matching rule at a delay of 1.5 s and for task performance at variable delays ranging from 10 to 90 s. From these findings we suggest that the tissue critical for auditory recognition memory is located outside both the perirhinal/entorhinal cortices and the hippocampus.