A preliminary analysis of the effect of individual differences on cognitive performance in young companion dogs.

Many factors influence cognitive performance in dogs, including breed, temperament, rearing history, and training. Studies in working dog populations have demonstrated age-related improvements in cognitive task performance across the first years of development. However, the effect of certain factors, such as age, sex, and temperament, on cognitive performance in puppies has yet to be evaluated in a more diverse population of companion dogs. In this study, companion dogs under 12 months of age were tested once on two tasks purported to measure aspects of executive function: the delayed-search task (DST) and the detour reversal task (DRT). Owners also filled out the Canine Behavioral Assessment and Research Questionnaire (C-BARQ) to evaluate how temperament influenced task performance. Contrary to prior research, performance did not improve with age on either task. However, the lack of age effects was likely the result of small sample sizes and individual differences across other factors influencing performance. Specifically, temperament differences as measured by the C-BARQ subscales for nonsocial fear and excitability predicted task performance on the DST, but the effect of temperament on task performance differed between males and females. Excitability also predicted performance on the DRT, but the effect depended on the age of the dog. In addition, no correlations were observed between task measures, indicating a lack of construct validity. Overall, these findings provide a preliminary analysis of factors that appear to influence cognitive task performance in young companion dogs and highlight suggestions for future research evaluating the impact of individual differences on cognitive performance.

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.

Human-dog relationships as a working framework for exploring human-robot attachment: a multidisciplinary review.

Robotic agents will be life-long companions of humans in the foreseeable future. To achieve such successful relationships, people will likely attribute emotions and personality, assign social competencies, and develop a long-lasting attachment to robots. However, without a clear theoretical framework-building on biological, psychological, and technological knowledge-current societal demands for establishing successful human-robot attachment (HRA) as a new form of inter-species interactions might fail. The study of evolutionarily adaptive animal behavior (i.e., ethology) suggests that human-animal behaviors can be considered as a plausible solution in designing and building models of ethorobots-including modeling the inter-species bond between domesticated animals and humans. Evidence shows that people assign emotional feelings and personality characteristics to animal species leading to cooperation and communication-crucial for designing social robots such as companion robots. Because dogs have excellent social skills with humans, current research applies human-dog relationships as a template to understand HRA. Our goal of this article is twofold. First, we overview the research on how human-dog interactions are implemented as prototypes of non-human social companions in HRA. Second, we review research about attitudes that humans have for interacting with robotic dogs based on their appearance and behavior, the implications for forming attachments, and human-animal interactions in the rising sphere of robot-assisted therapy. The rationale for this review is to provide a new perspective to facilitate future research among biologists, psychologists, and engineers-contributing to the creation of innovative research practices for studying social behaviors and its implications for society addressing HRA.

Dissociating the effects of delay and interference on dog (Canis familiaris) working memory.

Delayed matching-to-sample (dMTS) is commonly used to study working memory (WM) processes in non-humans. Previous procedures for studying dog WM, including versions of the dMTS, did not separate the impact of delay and interference on memory performance. These studies were also limited to auditory and spatial stimuli, neglecting dogs' dominant sensory modality (i.e., olfaction). Therefore, we designed the first olfactory dMTS in dogs, with systematically varied delays and number of odors in a session, to dissociate the effects of delay and within-session proactive interference on dog WM. Dogs (n = 5) initially trained on matching-to-sample with 48 odors, with a zero-second delay, were tested on four delay lengths (0, 30, 60, and 90 s), counterbalanced across three, trial-unique, sessions. Although there was a slight decrease in accuracy across delays, dogs performed above chance on delays up to 60 s, suggesting a WM duration of at least 60 s. To explore the effect of within-session proactive interference on WM duration, the size of the stimulus set was reduced to six and two odors. There was no effect on the memory function with six odors compared to the trial-unique sessions. However, the interference caused by the two-odor set was enough to decrease accuracy at each delay length. These findings suggest that forgetting in dog working memory for odors can be simultaneously influenced by delay and within-session proactive interference.

Dog-human social relationship: representation of human face familiarity and emotions in the dog brain.

This study investigated the behavioral and neural indices of detecting facial familiarity and facial emotions in human faces by dogs. Awake canine fMRI was used to evaluate dogs' neural response to pictures and videos of familiar and unfamiliar human faces, which contained positive, neutral, and negative emotional expressions. The dog-human relationship was behaviorally characterized out-of-scanner using an unsolvable task. The caudate, hippocampus, and amygdala, mainly implicated in reward, familiarity and emotion processing, respectively, were activated in dogs when viewing familiar and emotionally salient human faces. Further, the magnitude of activation in these regions correlated with the duration for which dogs showed human-oriented behavior towards a familiar (as opposed to unfamiliar) person in the unsolvable task. These findings provide a bio-behavioral basis for the underlying markers and functions of human-dog interaction as they relate to familiarity and emotion in human faces.

Dogs demonstrate memory of incidentally encoded information.

Fugazza, Pongrácz, Pogány, Lenkei, and Miklósi (Scientific Reports, 10(1), 1-8, 2020) recently showed that dogs can repeat incidentally encoded behaviors using unexpected tests. These results suggest that dogs may possess episodic-like memories for their own actions.

Same/different concept learning by primates and birds.

Same/different abstract-concept learning experiments were conducted with two primate species and three avian species by progressively increasing the size of the training stimulus set of distinctly different pictures from eight to 1,024 pictures. These same/different learning experiments were trained with two pictures presented simultaneously. Transfer tests of same and different learning employed interspersed trials of novel pictures to assess the level of correct performance on the very first time of subjects had seen those pictures. All of the species eventually performed these tests with high accuracy, contradicting the long-accepted notion that nonhuman animals are unable to learn the concept of same/different. Capuchin and rhesus monkeys learned the concept more readily than did pigeons. Clark's nutcrackers and black-billed magpies learned as readily as monkeys, and even showed a slight advantage with the smallest training stimulus sets. Those tests of same/different learning were followed by delay procedures, such that a delay was introduced after the subjects responded to the sample picture and before the test picture. In the sequential same/different task, accuracy was shown to diminish when the stimulus on a previous trial matched the test picture previously shown on a different trial. This effect is known as proactive interference. The pigeons' proactive interference was greater at 10-s delays than 1-s delays, revealing time-based interference. By contrast, time delays had little or no effect on rhesus monkeys' proactive interference, suggesting that rhesus monkeys have better explicit memory of where and when they saw the potential interfering picture, revealing better event-based memory.

Odor span task in dogs (Canis familiaris).

Working memory is essential for organisms to solve problems related to their survival and to adapt to changes in their environment. Researchers sought to create a non-human model of working memory that could be used to better understand its predictive value and underlying brain function. Several of these studies were conducted using the odor span task (OST) with rodents, and here, we present the first OST with domestic dogs (n = 6). The OST is an incrementing non-match-to-sample task in which dogs were presented with both a session novel (S +) and a previously encountered (S -) odor on each trial. A response to the session novel odor was always reinforced. Upon meeting training criterion on sessions with 24 trials or odors to remember, the dogs were tested on the OST with up to 72 odors to remember in the session. All dogs learned the OST and displayed accurate performance (≥ 79%) for the largest set size of 72 odors. In an analysis focused on the effect of intervening odors (i.e., the number of trials since the S - was last encountered), dogs demonstrated above-chance performance for up to eight intervening odors. The implications of these findings are discussed in the context of dog working memory for odors.

The development of problem-solving abilities in a population of candidate detection dogs (Canis familiaris).

Both ontogenetic and phylogenetic factors have shaped dogs' cognitive capabilities, resulting in a heightened social sensitivity at the apparent cost of non-social problem-solving abilities. Research has suggested that training history and life experience can influence problem-solving abilities in dogs. However, the ontogenetic development of problem-solving abilities in dogs has been less explored. We tested a population of candidate detection dogs of various ages across the first year of development on four well-established problem-solving tasks targeting different cognitive domains (i.e., cylinder, A-not-B barrier, delayed search, and spatial transposition tasks). We examined developmental effects by comparing cognitive task performance across three age groups. Age-related improvements for all four cognitive measures indicate developmental increases in processes related to inhibitory control, attention, and spatial cognition between 3 and 12 months of age. Additionally, we found some relationships between cognitive measures and detection dog performance measures, though effects were not as robust. We discuss the results in the context of canine cognitive development and corresponding effects of phylogeny and ontogeny, as well as potential applications to working dog training and selection.

Comparing pet and detection dogs (Canis familiaris) on two aspects of social cognition.

Interspecific communication between dogs and humans enables dogs to occupy significant roles in human society, both in companion and working roles. Dogs excel at using human communicative signals in problem-solving tasks, and solicit human contact when unable to solve a problem. Dogs' sociocognitive behavior likely results from a selection for attention to humans during domestication, but is highly susceptible to environmental factors. Training for particular tasks appears to enhance dog-human communication, but effects may depend on the nature of the relationship determined by their role. Our aim was to examine two types of social cognition (responsiveness to human gestures, and human-directed communicative behavior in an unsolvable task) in pet dogs (n = 29) and detection dogs (n = 35). The groups did not differ in their ability to follow human signals, but pets were less responsive to signals given by a stranger than by their owner. Pets also exhibited more human-directed gazing in the unsolvable task, showing a bias for gazing at their owner compared with the stranger, whereas detection dogs showed greater persistence in attempting to solve the task compared with pets. Thus, different aspects of dogs' sociocognitive behavior may differentially vary as a function of selection or training for particular roles.

Identifying disease foci from static and dynamic effective connectivity networks: Illustration in soldiers with trauma.

Brain connectivity studies report group differences in pairwise connection strengths. While informative, such results are difficult to interpret since our understanding of the brain relies on region-based properties, rather than on connection information. Given that large disruptions in the brain are often caused by a few pivotal sources, we propose a novel framework to identify the sources of functional disruption from effective connectivity networks. Our approach integrates static and time-varying effective connectivity modeling in a probabilistic framework, to identify aberrant foci and the corresponding aberrant connectomics network. Using resting-state fMRI, we illustrate the utility of this novel approach in U.S. Army soldiers (N = 87) with posttraumatic stress disorder (PTSD), mild traumatic brain injury (mTBI) and combat controls. Additionally, we employed machine-learning classification to identify those significant connectivity features that possessed high predictive ability. We identified three disrupted foci (middle frontal gyrus [MFG], insula, hippocampus), and an aberrant prefrontal-subcortical-parietal network of information flow. We found the MFG to be the pivotal focus of network disruption, with aberrant strength and temporal-variability of effective connectivity to the insula, amygdala and hippocampus. These connectivities also possessed high predictive ability (giving a classification accuracy of 81%); and they exhibited significant associations with symptom severity and neurocognitive functioning. In summary, dysregulation originating in the MFG caused elevated and temporally less-variable connectivity in subcortical regions, followed by a similar effect on parietal memory-related regions. This mechanism likely contributes to the reduced control over traumatic memories leading to re-experiencing, hyperarousal and flashbacks observed in soldiers with PTSD and mTBI. Hum Brain Mapp 39:264-287, 2018. © 2017 Wiley Periodicals, Inc.

Mothering matters: Maternal style predicts puppies' future performance.

Bray et al. (2017, Proceedings of the National Academy of Sciences, 113(32), 9128-9133) recently showed that maternal interactions between service dog mothers and their puppies were predictive of puppies' future success as a candidate service dog. These findings prompt questions into the role of genetics and early experiences and may provide useful selection tools for working dog breeding programs.

Comparing cognition by integrating concept learning, proactive interference, and list memory.

This article describes an approach for training a variety of species to learn the abstract concept of same/different, which in turn forms the basis for testing proactive interference and list memory. The stimulus set for concept-learning training was progressively doubled from 8, 16, 32, 64, 128 . . . to 1,024 different pictures with novel-stimulus transfer following learning. All species fully learned the same/different abstract concept: capuchin and rhesus monkeys learned more readily than pigeons; nutcrackers and magpies were at least equivalent to monkeys and transferred somewhat better following initial training sets. A similar task using the 1,024-picture set plus delays was used to test proactive interference on occasional trials. Pigeons revealed greater interference with 10-s than with 1-s delays, whereas delay time had no effect on rhesus monkeys, suggesting that the monkeys' interference was event based. This same single-item same/different task was expanded to a 4-item list memory task to test animal list memory. Humans were tested similarly with lists of kaleidoscope pictures. Delays between the list and test were manipulated, resulting in strong initial recency effects (i.e., strong 4th-item memory) at short delays and changing to a strong primacy effect (i.e., strong 1st-item memory) at long delays (pigeons 0-s to 10-s delays; monkeys 0-s to 30-s delays; humans 0-s to 100-s delays). Results and findings are discussed in terms of these species' cognition and memory comparisons, evolutionary implications, and future directions for testing other species in these synergistically related tasks.

Separate brain areas for processing human and dog faces as revealed by awake fMRI in dogs (Canis familiaris).

Functional magnetic resonance imaging (fMRI) has emerged as a viable method to study the neural processing underlying cognition in awake dogs. Working dogs were presented with pictures of dog and human faces. The human faces varied in familiarity (familiar trainers and unfamiliar individuals) and emotional valence (negative, neutral, and positive). Dog faces were familiar (kennel mates) or unfamiliar. The findings revealed adjacent but separate brain areas in the left temporal cortex for processing human and dog faces in the dog brain. The human face area (HFA) and dog face area (DFA) were both parametrically modulated by valence indicating emotion was not the basis for the separation. The HFA and DFA were not influenced by familiarity. Using resting state fMRI data, functional connectivity networks (connectivity fingerprints) were compared and matched across dogs and humans. These network analyses found that the HFA mapped onto the human fusiform area and the DFA mapped onto the human superior temporal gyrus, both core areas in the human face processing system. The findings provide insight into the evolution of face processing.

Compromised hippocampus-striatum pathway as a potential imaging biomarker of mild-traumatic brain injury and posttraumatic stress disorder.

OBJECTIVES: Military service members risk acquiring posttraumatic stress disorder (PTSD) and mild-traumatic brain injury (mTBI), with high comorbidity. Owing to overlapping symptomatology in chronic mTBI or postconcussion syndrome (PCS) and PTSD, it is difficult to assess the etiology of a patient's condition without objective measures. Using resting-state functional MRI in a novel framework, we tested the hypothesis that their neural signatures are characterized by functionally hyperconnected brain regions which are less variable over time. Additionally, we predicted that such connectivities possessed the highest ability in predicting the diagnostic membership of a novel subject (top-predictors) in addition to being statistically significant. METHODS: U.S. Army Soldiers (N = 87) with PTSD and comorbid PCS + PTSD were recruited along with combat controls. Static and dynamic functional connectivities were evaluated. Group differences were obtained in accordance with our hypothesis. Machine learning classification (MLC) was employed to determine top predictors. RESULTS: From whole-brain connectivity, we identified the hippocampus-striatum connectivity to be significantly altered in accordance with our hypothesis. Diffusion tractography revealed compromised white-matter integrity between aforementioned regions only in the PCS + PTSD group, suggesting a structural etiology for the PCS + PTSD group rather than being an extreme subset of PTSD. Employing MLC, connectivities provided worst-case accuracy of 84% (9% more than psychological measures). Additionally, the hippocampus-striatum connectivities were found to be top predictors and thus a potential biomarker of PTSD/mTBI. CONCLUSIONS: PTSD/mTBI are associated with hippocampal-striatal hyperconnectivity from which it is difficult to disengage, leading to a habit-like response toward episodic traumatic memories, which fits well with behavioral manifestations of combat-related PTSD/mTBI. Hum Brain Mapp 38:2843-2864, 2017. © 2017 The Authors Human Brain Mapping Published by Wiley Periodicals, Inc.

Corvids Outperform Pigeons and Primates in Learning a Basic Concept.

Corvids (birds of the family Corvidae) display intelligent behavior previously ascribed only to primates, but such feats are not directly comparable across species. To make direct species comparisons, we used a same/different task in the laboratory to assess abstract-concept learning in black-billed magpies ( Pica hudsonia). Concept learning was tested with novel pictures after training. Concept learning improved with training-set size, and test accuracy eventually matched training accuracy-full concept learning-with a 128-picture set; this magpie performance was equivalent to that of Clark's nutcrackers (a species of corvid) and monkeys (rhesus, capuchin) and better than that of pigeons. Even with an initial 8-item picture set, both corvid species showed partial concept learning, outperforming both monkeys and pigeons. Similar corvid performance refutes the hypothesis that nutcrackers' prolific cache-location memory accounts for their superior concept learning, because magpies rely less on caching. That corvids with "primitive" neural architectures evolved to equal primates in full concept learning and even to outperform them on the initial 8-item picture test is a testament to the shared (convergent) survival importance of abstract-concept learning.

The oddity preference effect and the concept of difference in pigeons.

Previous work in discrimination learning has shown that nonmatching (oddity) tasks are learned faster and more accurately than comparable matching tasks. This learning advantage has been coined the oddity preference effect (Wright & Delius in Journal of Experimental Psychology: Animal Behavior Processes, 31, 425-432. doi: 10.1037/0097-7403.31.4.425 , 2005). Pigeons trained in a nonmatching task, following training in a same/different (S/D) task, learned the abstract concept of difference (Daniel et al., in Animal Cognition, 18(4), 831-837, 2015), but they did not show the expected faster acquisition or high levels of transfer from the oddity preference effect. In the present study, experimentally naïve pigeons were trained in an identical nonmatching task to examine whether they would show the oddity preference effect on abstract-concept learning. These experimentally naïve pigeons did show an oddity preference effect; their transfer to novel configurations was above chance with the initial (smallest) set size (3-item set) and was substantially more accurate than novel transfer in similar match-to-sample (MTS) or S/D tasks (Bodily et al., in Journal of Experimental Psychology: Animal Behavior Processes, 34, 178-184. doi: 10.1037/0097-7403.34.1.178 , 2008; Katz & Wright in Journal of Experimental Psychology: Animal Behavior Processes, 32, 80-86. doi: 10.1037/0097-7403.32.1.80 , 2006). As the number exemplars in the training set increased, transfer to novel configurations increased and reached equivalence to trained-stimulus performance with a 24-item set. Despite this transfer being equal to baseline performance with a 24-item set, subsequent transfers following training with larger set sizes declined before eventually rising again to baseline performance. This unusual set-size function (with inflection points at the 24- and 96-set sizes) suggests that these pigeons may have combined item-specific and relational learning strategies with differing emphasis as they acquired the abstract concept.

Neurofunctional topography of the human hippocampus.

Much of what was assumed about the functional topography of the hippocampus was derived from a single case study over half a century ago. Given advances in the imaging sciences, a new era of discovery is underway, with potential to transform the understanding of healthy processing as well as the ability to treat disorders. Coactivation-based parcellation, a meta-analytic approach, and ultra-high field, high-resolution functional and structural neuroimaging to characterize the neurofunctional topography of the hippocampus was employed. Data revealed strong support for an evolutionarily preserved topography along the long-axis. Specifically, the left hippocampus was segmented into three distinct clusters: an emotional processing cluster supported by structural and functional connectivity to the amygdala and parahippocampal gyrus, a cognitive operations cluster, with functional connectivity to the anterior cingulate and inferior frontal gyrus, and a posterior perceptual cluster with distinct structural connectivity patterns to the occipital lobe coupled with functional connectivity to the precuneus and angular gyrus. The right hippocampal segmentation was more ambiguous, with plausible 2- and 5-cluster solutions. Segmentations shared connectivity with brain regions known to support the correlated processes. This represented the first neurofunctional topographic model of the hippocampus using a robust, bias-free, multimodal approach.

Abstract-concept learning of difference in pigeons.

Many species have demonstrated the capacity to learn abstract concepts. Recent studies have shown that the quantity of stimuli used during training plays a critical role in how subjects learn abstract concepts. As the number of stimuli available in the training set increases, so too does performance on novel combinations. The role of set size has been explored with learning the concept of matching and same/different but not with learning the concept of difference. In the present study, pigeons were trained in a non-matching-to-sample task with an initial training set of three stimuli followed by transfer tests to novel stimuli. The training set was progressively doubled eight times with learning and transfer following each expansion. Transfer performance increased from chance level (50 %) at the smallest set size to a level equivalent to asymptotic training performance at the two largest training set sizes (384, 768). This progressive novel-stimulus transfer function of a non-matching (difference) rule is discussed in comparison with results from a similar experiment where pigeons were trained on a matching rule.