An Ecological and Neural Argument for Developing Pursuit-Based Cognitive Enrichment for Sea Lions in Human Care.

While general enrichment strategies for captive animals attempt to elicit variable and species-typical behaviors, approaches to cognitive enrichment have been disappointingly one-size-fits-all. In this commentary, we address the potential benefit of tailoring cognitive enrichment to the "cognitive niche" of the species, with a particular focus on a reasonably well-studied marine carnivore, the sea lion. Sea lions likely share some cognitive evolutionary pressures with primates, including complex social behavior. Their foraging ecology, however, like that of many terrestrial carnivores, is based on the rapid and behaviorally flexible pursuit of avoidant prey. Unlike terrestrial carnivores, sea lions carry out this pursuit in a truly fluid three-dimensional field, computing and executing sensorimotor transformations from any solid angle to any other. The cognitive demands of flexible prey pursuit are unlikely to be fully elicited by typical stationary puzzle box style foraging enrichment devices or screen-based interactive games. With this species, we recommend exploring more water-based movement activities generally, and complex pursuit challenges specifically.

Volumetric and connectivity assessment of the caudate nucleus in California sea lions and coyotes.

In addition to a large (chimpanzee-sized) and heavily convoluted brain, one of the most striking neurobiological features in pinnipeds is the large size of the head of the caudate nucleus, which dwarfs the rest of the striatum. Although previous research has suggested carnivore striatum is small in comparison to that of primates, there are limited volumetric data on separate striatal structures in carnivores. Therefore, the apparent functional implication of a potentially hypertrophic caudate to carnivores has not been discussed. Here, for the first time, we obtained separate volumetric measurements of caudate and putamen in California sea lions and coyotes. Exemplars of both species had very large caudate nuclei, approximately 1/75th of total brain volume. In both the sea lion and coyote, the caudate dwarfed the putamen at a ratio of 13 to 1 or greater, a finding in strong contrast to measurements showing larger putamen than caudate in primates. In addition, using post-mortem diffusion tensor brain imaging, we mapped and compared white matter connections between the dorsal caudate and the motor, premotor and frontopolar, and orbitofrontal cortices in healthy adult sea lions and healthy adult coyotes. The sea lions showed some evidence of greater premotor and frontopolar connectivity. These findings bear on previously underexplored striatal characteristics of large carnivores, and we discuss potential interpretations related to cognitive flexibility and sensorimotor transformation.

An ecological approach to measuring synchronization abilities across the animal kingdom.

In this perspective paper, we focus on the study of synchronization abilities across the animal kingdom. We propose an ecological approach to studying nonhuman animal synchronization that begins from observations about when, how and why an animal might synchronize spontaneously with natural environmental rhythms. We discuss what we consider to be the most important, but thus far largely understudied, temporal, physical, perceptual and motivational constraints that must be taken into account when designing experiments to test synchronization in nonhuman animals. First and foremost, different species are likely to be sensitive to and therefore capable of synchronizing at different timescales. We also argue that it is fruitful to consider the latent flexibility of animal synchronization. Finally, we discuss the importance of an animal's motivational state for showcasing synchronization abilities. We demonstrate that the likelihood that an animal can successfully synchronize with an environmental rhythm is context-dependent and suggest that the list of species capable of synchronization is likely to grow when tested with ecologically honest, species-tuned experiments. This article is part of the theme issue 'Synchrony and rhythm interaction: from the brain to behavioural ecology'.

An MRI protocol for anatomical and functional evaluation of the California sea lion brain.

BACKGROUND: Domoic acid (DOM) is a neurotoxin produced by some harmful algae blooms in coastal waters. California sea lions (Zalophus californianus) exposed to DOM often strand on beaches where they exhibit a variety of symptoms, including seizures. These animals typically show hippocampal atrophy on MRI scans. NEW METHOD: We describe an MRI protocol for comprehensive evaluation of DOM toxicosis in the sea lion brain. We intend to study brain development in pups exposed in utero. The protocol depicts the hippocampal formation as the primary region of interest. We include scans for quantitative morphometry, functional and structural connectivity, and a cerebral blood flow map. RESULTS: High-resolution 3D anatomical scans facilitate post hoc slicing in arbitrary planes and accurate morphometry. We demonstrate the first cerebral blood flow map using MRI, and the first structural tractography from a live sea lion brain. COMPARISON WITH EXISTING METHODS: Scans were compared to prior anatomical and functional studies in live sea lions, and structural connectivity in post mortem specimens. Hippocampal volumes were broadly in line with prior studies, with differences likely attributable to the 3D approach used here. Functional connectivity of the dorsal left hippocampus matched that found in a prior study conducted at a lower magnetic field, while structural connectivity in the live brain agreed with findings observed in post mortem studies. CONCLUSIONS: Our protocol provides a comprehensive, longitudinal view of the functional and anatomical changes expected to result from DOM toxicosis. It can also screen for other common neurological pathologies and is suitable for any pinniped that can fit inside an MRI scanner.

The Relevance of Ecological Transitions to Intelligence in Marine Mammals.

Macphail's comparative approach to intelligence focused on associative processes, an orientation inconsistent with more multifaceted lay and scientific understandings of the term. His ultimate emphasis on associative processes indicated few differences in intelligence among vertebrates. We explore options more attuned to common definitions by considering intelligence in terms of richness of representations of the world, the interconnectivity of those representations, the ability to flexibly change those connections, and knowledge. We focus on marine mammals, represented by the amphibious pinnipeds and the aquatic cetaceans and sirenians, as animals that transitioned from a terrestrial existence to an aquatic one, experiencing major changes in ecological pressures. They adapted with morphological transformations related to streamlining the body, physiological changes in respiration and thermoregulation, and sensory/perceptual changes, including echolocation capabilities and diminished olfaction in many cetaceans, both in-air and underwater visual focus, and enhanced senses of touch in pinnipeds and sirenians. Having a terrestrial foundation on which aquatic capacities were overlaid likely affected their cognitive abilities, especially as a new reliance on sound and touch, and the need to surface to breath changed their interactions with the world. Vocal and behavioral observational learning capabilities in the wild and in laboratory experiments suggest versatility in group coordination. Empirical reports on aspects of intelligent behavior like problem-solving, spatial learning, and concept learning by various species of cetaceans and pinnipeds suggest rich cognitive abilities. The high energy demands of the brain suggest that brain-intelligence relationships might be fruitful areas for study when specific hypotheses are considered, e.g., brain mapping indicates hypertrophy of specific sensory areas in marine mammals. Modern neuroimaging techniques provide ways to study neural connectivity, and the patterns of connections between sensory, motor, and other cortical regions provide a biological framework for exploring how animals represent and flexibly use information in navigating and learning about their environment. At this stage of marine mammal research, it would still be prudent to follow Macphail's caution that it is premature to make strong comparative statements without more empirical evidence, but an approach that includes learning more about how animals flexibly link information across multiple representations could be a productive way of comparing species by allowing them to use their specific strengths within comparative tasks.

Awake fMRI Reveals Brain Regions for Novel Word Detection in Dogs.

How do dogs understand human words? At a basic level, understanding would require the discrimination of words from non-words. To determine the mechanisms of such a discrimination, we trained 12 dogs to retrieve two objects based on object names, then probed the neural basis for these auditory discriminations using awake-fMRI. We compared the neural response to these trained words relative to "oddball" pseudowords the dogs had not heard before. Consistent with novelty detection, we found greater activation for pseudowords relative to trained words bilaterally in the parietotemporal cortex. To probe the neural basis for representations of trained words, searchlight multivoxel pattern analysis (MVPA) revealed that a subset of dogs had clusters of informative voxels that discriminated between the two trained words. These clusters included the left temporal cortex and amygdala, left caudate nucleus, and thalamus. These results demonstrate that dogs' processing of human words utilizes basic processes like novelty detection, and for some dogs, may also include auditory and hedonic representations.

Postmortem DTI reveals altered hippocampal connectivity in wild sea lions diagnosed with chronic toxicosis from algal exposure.

Hundreds of wild California sea lions (Zalophus californianus) exposed to the algal neurotoxin domoic acid are treated in veterinary rehabilitation centers each year. Common chronic effects of toxic exposure in these animals are seizures and hippocampal damage, and they have been proposed as a natural animal model for human epilepsy. Humans with medial temporal lobe epilepsy present with white matter pathology in a number of tracts including the fornix and increased structural connectivity between the hippocampus and thalamus. However, there are no prior data on structural connectivity in sea lion brains, with or without neuropathology. In the present study, we used a novel diffusion tensor imaging technique to obtain high resolution (1mm isotropic) white matter maps in brains obtained opportunistically postmortem from wild sea lions with and without chronic clinical signs of toxic exposure to domoic acid. All animals had received a full veterinary workup and diagnosis prior to euthanasia. We measured hippocampal atrophy morphometrically, and all brains were examined histopathologically. In animals diagnosed with chronic domoic acid toxicosis, the fornix showed signs of altered diffusion properties indicative of pathology; these brains also had increased structural connectivity between hippocampus and thalamus in comparison to brains from animals with no neurological signs. These findings establish further parallels between human medial temporal lobe epilepsy and a naturally occurring condition in wild sea lions and simultaneously advance general knowledge of the deleterious effects of an increasingly common natural toxin.

The evolutionary biology of dance without frills.

Recently psychologists have taken up the question of whether dance is reliant on unique human adaptations, or whether it is rooted in neural and cognitive mechanisms shared with other species [1,2]. In its full cultural complexity, human dance clearly has no direct analog in animal behavior. Most definitions of dance include the consistent production of movement sequences timed to an external rhythm. While not sufficient for dance, modes of auditory-motor timing, such as synchronization and entrainment, are experimentally tractable constructs that may be analyzed and compared between species. In an effort to assess the evolutionary precursors to entrainment and social features of human dance, Laland and colleagues [2] have suggested that dance may be an incidental byproduct of adaptations supporting vocal or motor imitation - referred to here as the 'imitation and sequencing' hypothesis. In support of this hypothesis, Laland and colleagues rely on four convergent lines of evidence drawn from behavioral and neurobiological research on dance behavior in humans and rhythmic behavior in other animals. Here, we propose a less cognitive, more parsimonious account for the evolution of dance. Our 'timing and interaction' hypothesis suggests that dance is scaffolded off of broadly conserved timing mechanisms allowing both cooperative and antagonistic social coordination.

Awake canine fMRI predicts dogs' preference for praise vs food.

Dogs are hypersocial with humans, and their integration into human social ecology makes dogs a unique model for studying cross-species social bonding. However, the proximal neural mechanisms driving dog-human social interaction are unknown. We used functional magnetic resonance imaging in 15 awake dogs to probe the neural basis for their preferences for social interaction and food reward. In a first experiment, we used the ventral caudate as a measure of intrinsic reward value and compared activation to conditioned stimuli that predicted food, praise or nothing. Relative to the control stimulus, the caudate was significantly more active to the reward-predicting stimuli and showed roughly equal or greater activation to praise vs food in 13 of 15 dogs. To confirm that these differences were driven by the intrinsic value of social praise, we performed a second imaging experiment in which the praise was withheld on a subset of trials. The difference in caudate activation to the receipt of praise, relative to its withholding, was strongly correlated with the differential activation to the conditioned stimuli in the first experiment. In a third experiment, we performed an out-of-scanner choice task in which the dog repeatedly selected food or owner in a Y-maze. The relative caudate activation to food- and praise-predicting stimuli in Experiment 1 was a strong predictor of each dog's sequence of choices in the Y-maze. Analogous to similar neuroimaging studies of individual differences in human social reward, our findings demonstrate a neural mechanism for preference in domestic dogs that is stable within, but variable between, individuals. Moreover, the individual differences in the caudate responses indicate the potentially higher value of social than food reward for some dogs and may help to explain the apparent efficacy of social interaction in dog training.

Natural exposure to domoic acid causes behavioral perseveration in Wild Sea lions: Neural underpinnings and diagnostic application.

Domoic acid is a naturally occurring algal toxin that causes neurological symptoms and mortality in exposed marine life. California sea lions (Zalophus californianus) are the most visible victims, and suffer epilepsy and progressive hippocampal atrophy. Despite its reliable neurological effects, little is known about how exposure to domoic acid alters behavior, which is critical for understanding the impact of toxic exposure on long-term survival in sea lions and other exposed animals, including humans. Better understanding of the behavioral effects may also inform veterinary diagnosis and treatment. Anecdotally, exposed sea lions have been reported to show enhanced perseverative behavior. To assess the neurobehavioral effects of domoic acid, we compared veterinary diagnoses, measures of hippocampal volume from in vivo MRI, and behavioral measures of habituation and dishabituation in 27 wild sea lions undergoing rehabilitation. The sample was divided post-hoc between subjects with clear veterinary diagnoses of chronic domoic acid toxicosis and those with no evidence of the disease. In the behavioral task, subjects were exposed repeatedly to sounds from two source locations, and, following a short delay, exposed again. Veterinary diagnosis of domoic acid toxicosis was associated with extent of hippocampal damage, predicted delayed habituation in phase 1, and enhanced dishabituation in phase 2. Receiver operating characteristic analysis indicated that delayed habituation in phase 1 was diagnostically predictive. Enhanced dishabituation in phase 2 was correlated with reduced right ventral hippocampal volume. Together, delayed habituation and enhanced dishabituation following domoic acid exposure indicate a clinically relevant and potentially maladaptive behavioral pattern of perseveration.

Beat Keeping in a Sea Lion As Coupled Oscillation: Implications for Comparative Understanding of Human Rhythm.

Human capacity for entraining movement to external rhythms-i.e., beat keeping-is ubiquitous, but its evolutionary history and neural underpinnings remain a mystery. Recent findings of entrainment to simple and complex rhythms in non-human animals pave the way for a novel comparative approach to assess the origins and mechanisms of rhythmic behavior. The most reliable non-human beat keeper to date is a California sea lion, Ronan, who was trained to match head movements to isochronous repeating stimuli and showed spontaneous generalization of this ability to novel tempos and to the complex rhythms of music. Does Ronan's performance rely on the same neural mechanisms as human rhythmic behavior? In the current study, we presented Ronan with simple rhythmic stimuli at novel tempos. On some trials, we introduced "perturbations," altering either tempo or phase in the middle of a presentation. Ronan quickly adjusted her behavior following all perturbations, recovering her consistent phase and tempo relationships to the stimulus within a few beats. Ronan's performance was consistent with predictions of mathematical models describing coupled oscillation: a model relying solely on phase coupling strongly matched her behavior, and the model was further improved with the addition of period coupling. These findings are the clearest evidence yet for parity in human and non-human beat keeping and support the view that the human ability to perceive and move in time to rhythm may be rooted in broadly conserved neural mechanisms.

Neurobehavioral evidence for individual differences in canine cognitive control: an awake fMRI study.

Based on behavioral evidence, the domestic dog has emerged as a promising comparative model of human self-control. However, while research on human inhibition has probed heterogeneity and neuropathology through an integration of neural and behavioral evidence, there are no parallel data exploring the brain mechanisms involved in canine inhibition. Here, using a combination of cognitive testing and awake neuroimaging in domestic dogs, we provide evidence precisely localizing frontal brain regions underpinning response inhibition in this species and demonstrate the dynamic relationship between these regions and behavioral measures of control. Thirteen dogs took part in an in-scanner go/no-go task and an out-of-scanner A-not-B test. A frontal brain region was identified showing elevated neural activity for all subjects during successful inhibition in the scanner, and dogs showing greater mean brain activation in this region produced fewer false alarms. Better performance in the go/no-go task was also correlated with fewer errors in the out-of-scanner A-not-B test, suggesting that dogs show consistent neurobehavioral individual differences in cognitive control, as is seen in humans. These findings help establish parity between human and canine mechanisms of self-control and pave the way for future comparative studies examining their function and dysfunction.

Rhythmic entrainment: Why humans want to, fireflies can't help it, pet birds try, and sea lions have to be bribed.

Until recently, the literature on rhythmic ability took for granted that only humans are able to synchronize body movements to an external beat-to entrain. This assumption has been undercut by findings of beat-matching in various species of parrots and, more recently, in a sea lion, several species of primates, and possibly horses. This throws open the question of how widespread beat-matching ability is in the animal kingdom. Here we reassess the arguments and evidence for an absence of beat-matching in animals, and conclude that in fact no convincing case against beat-matching in animals has been made. Instead, such evidence as there is suggests that this capacity could be quite widespread. Furthermore, mutual entrainment of oscillations is a general principle of physical systems, both biological and nonbiological, suggesting that entrainment of motor systems by sensory systems may be a default rather than an oddity. The question then becomes, not why a few privileged species are able to beat-match, but why species do not always do so-why they vary in both spontaneous and learned beat-matching. We propose that when entrainment is not driven by fixed, mandatory connections between input and output (as in the case of, e.g., fireflies entraining to each others' flashes), it depends on voluntary control over, and voluntary or learned coupling of, sensory and motor systems, which can paradoxically lead to apparent failures of entrainment. Among the factors that affect whether an animal will entrain are sufficient control over the motor behavior to be entrained, sufficient perceptual sophistication to extract the entraining beat from the overall sensory environment, and the current cognitive state of the animal, including attention and motivation. The extent of entrainment in the animal kingdom potentially has widespread implications, not only for understanding the roots of human dance, but also for understanding the neural and cognitive architectures of animals.

Algal toxin impairs sea lion memory and hippocampal connectivity, with implications for strandings.

Domoic acid (DA) is a naturally occurring neurotoxin known to harm marine animals. DA-producing algal blooms are increasing in size and frequency. Although chronic exposure is known to produce brain lesions, the influence of DA toxicosis on behavior in wild animals is unknown. We showed, in a large sample of wild sea lions, that spatial memory deficits are predicted by the extent of right dorsal hippocampal lesions related to natural exposure to DA and that exposure also disrupts hippocampal-thalamic brain networks. Because sea lions are dynamic foragers that rely on flexible navigation, impaired spatial memory may affect survival in the wild.

Diffusion tensor imaging of dolphin brains reveals direct auditory pathway to temporal lobe.

The brains of odontocetes (toothed whales) look grossly different from their terrestrial relatives. Because of their adaptation to the aquatic environment and their reliance on echolocation, the odontocetes' auditory system is both unique and crucial to their survival. Yet, scant data exist about the functional organization of the cetacean auditory system. A predominant hypothesis is that the primary auditory cortex lies in the suprasylvian gyrus along the vertex of the hemispheres, with this position induced by expansion of 'associative' regions in lateral and caudal directions. However, the precise location of the auditory cortex and its connections are still unknown. Here, we used a novel diffusion tensor imaging (DTI) sequence in archival post-mortem brains of a common dolphin (Delphinus delphis) and a pantropical dolphin (Stenella attenuata) to map their sensory and motor systems. Using thalamic parcellation based on traditionally defined regions for the primary visual (V1) and auditory cortex (A1), we found distinct regions of the thalamus connected to V1 and A1. But in addition to suprasylvian-A1, we report here, for the first time, the auditory cortex also exists in the temporal lobe, in a region near cetacean-A2 and possibly analogous to the primary auditory cortex in related terrestrial mammals (Artiodactyla). Using probabilistic tract tracing, we found a direct pathway from the inferior colliculus to the medial geniculate nucleus to the temporal lobe near the sylvian fissure. Our results demonstrate the feasibility of post-mortem DTI in archival specimens to answer basic questions in comparative neurobiology in a way that has not previously been possible and shows a link between the cetacean auditory system and those of terrestrial mammals. Given that fresh cetacean specimens are relatively rare, the ability to measure connectivity in archival specimens opens up a plethora of possibilities for investigating neuroanatomy in cetaceans and other species.

One pair of hands is not like another: caudate BOLD response in dogs depends on signal source and canine temperament.

Having previously used functional MRI to map the response to a reward signal in the ventral caudate in awake unrestrained dogs, here we examined the importance of signal source to canine caudate activation. Hand signals representing either incipient reward or no reward were presented by a familiar human (each dog's respective handler), an unfamiliar human, and via illustrated images of hands on a computer screen to 13 dogs undergoing voluntary fMRI. All dogs had received extensive training with the reward and no-reward signals from their handlers and with the computer images and had minimal exposure to the signals from strangers. All dogs showed differentially higher BOLD response in the ventral caudate to the reward versus no reward signals, and there was a robust effect at the group level. Further, differential response to the signal source had a highly significant interaction with a dog's general aggressivity as measured by the C-BARQ canine personality assessment. Dogs with greater aggressivity showed a higher differential response to the reward signal versus no-reward signal presented by the unfamiliar human and computer, while dogs with lower aggressivity showed a higher differential response to the reward signal versus no-reward signal from their handler. This suggests that specific facets of canine temperament bear more strongly on the perceived reward value of relevant communication signals than does reinforcement history, as each of the dogs were reinforced similarly for each signal, regardless of the source (familiar human, unfamiliar human, or computer). A group-level psychophysiological interaction (PPI) connectivity analysis showed increased functional coupling between the caudate and a region of cortex associated with visual discrimination and learning on reward versus no-reward trials. Our findings emphasize the sensitivity of the domestic dog to human social interaction, and may have other implications and applications pertinent to the training and assessment of working and pet dogs.