Putative neural consequences of captivity for elephants and cetaceans.

The present review assesses the potential neural impact of impoverished, captive environments on large-brained mammals, with a focus on elephants and cetaceans. These species share several characteristics, including being large, wide-ranging, long-lived, cognitively sophisticated, highly social, and large-brained mammals. Although the impact of the captive environment on physical and behavioral health has been well-documented, relatively little attention has been paid to the brain itself. Here, we explore the potential neural consequences of living in captive environments, with a focus on three levels: (1) The effects of environmental impoverishment/enrichment on the brain, emphasizing the negative neural consequences of the captive/impoverished environment; (2) the neural consequences of stress on the brain, with an emphasis on corticolimbic structures; and (3) the neural underpinnings of stereotypies, often observed in captive animals, underscoring dysregulation of the basal ganglia and associated circuitry. To this end, we provide a substantive hypothesis about the negative impact of captivity on the brains of large mammals (e.g., cetaceans and elephants) and how these neural consequences are related to documented evidence for compromised physical and psychological well-being.

Third time's the charm or three strikes you're out? An updated review of the efficacy of dolphin-assisted therapy for autism and developmental disabilities.

CONTEXT: Dolphin-assisted therapy (DAT) is a popular form of animal-assisted therapy for autism spectrum disorders and other psychological conditions. OBJECTIVE: In this review, our third, we analyze the most recent DAT studies in terms of construct and internal validity criteria to determine if there is empirical support for DAT. METHOD: To ensure a systematic review, we searched for peer-reviewed studies on DAT by submitting relevant search terms to Google Scholar from 2007 to 2020, conducted a further search of all DAT papers in several peer-reviewed journals, and reviewed reference sections of DAT articles to ensure a thorough review of the literature between 2007 and the present. RESULTS: The DAT literature continues to be marked by several weaknesses in both internal and construct validity that preclude confident inferences regarding the intervention's efficacy. CONCLUSION: There is still insufficient evidence that DAT has therapeutic value.

Thinking chickens: a review of cognition, emotion, and behavior in the domestic chicken.

Domestic chickens are members of an order, Aves, which has been the focus of a revolution in our understanding of neuroanatomical, cognitive, and social complexity. At least some birds are now known to be on par with many mammals in terms of their level of intelligence, emotional sophistication, and social interaction. Yet, views of chickens have largely remained unrevised by this new evidence. In this paper, I examine the peer-reviewed scientific data on the leading edge of cognition, emotions, personality, and sociality in chickens, exploring such areas as self-awareness, cognitive bias, social learning and self-control, and comparing their abilities in these areas with other birds and other vertebrates, particularly mammals. My overall conclusion is that chickens are just as cognitively, emotionally and socially complex as most other birds and mammals in many areas, and that there is a need for further noninvasive comparative behavioral research with chickens as well as a re-framing of current views about their intelligence.

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.

Autism, lateralisation, and handedness: a review of the literature and meta-analysis.

A number of recent investigators have hypothesised a link between autism, left-handedness, and brain laterality. Their findings have varied widely, in part because these studies have relied on different methodologies and definitions. We conducted a systematic review and meta-analysis to assess the literature, with the hypothesis that there would be an association between autism and laterality that would be moderated by handedness, sex, age, brain region studied, and level of autism. From a broad search resulting in 259 papers, 54 were identified for inclusion in the literature review. This list was narrowed further to include only studies reporting results in the inferior frontal gyrus for meta-analysis, resulting in four papers. The meta-analysis found a moderate but non-significant effect size of group on lateralisation, suggesting a decrease in strength of lateralisation in the autistic group, a trend supported by the literature review. A subgroup analysis of sex and a meta-regression of handedness showed that these moderating variables did not have a significant effect on this relationship. Although the results are not conclusive, there appears to be a trend towards a relationship between autism and lateralisation. However, more rigorous studies with better controls and clearer reporting of definitions and results are needed.

The evolutionary history of cetacean brain and body size.

Cetaceans rival primates in brain size relative to body size and include species with the largest brains and biggest bodies to have ever evolved. Cetaceans are remarkably diverse, varying in both phenotypes by several orders of magnitude, with notable differences between the two extant suborders, Mysticeti and Odontoceti. We analyzed the evolutionary history of brain and body mass, and relative brain size measured by the encephalization quotient (EQ), using a data set of extinct and extant taxa to capture temporal variation in the mode and direction of evolution. Our results suggest that cetacean brain and body mass evolved under strong directional trends to increase through time, but decreases in EQ were widespread. Mysticetes have significantly lower EQs than odontocetes due to a shift in brain:body allometry following the divergence of the suborders, caused by rapid increases in body mass in Mysticeti and a period of body mass reduction in Odontoceti. The pattern in Cetacea contrasts with that in primates, which experienced strong trends to increase brain mass and relative brain size, but not body mass. We discuss what these analyses reveal about the convergent evolution of large brains, and highlight that until recently the most encephalized mammals were odontocetes, not primates.

Towards a new paradigm of non-captive research on cetacean cognition.

Contemporary knowledge of impressive neurophysiology and behavior in cetaceans, combined with increasing opportunities for studying free-ranging cetaceans who initiate sociable interaction with humans, are converging to highlight serious ethical considerations and emerging opportunities for a new era of progressive and less-invasive cetacean research. Most research on cetacean cognition has taken place in controlled captive settings, e.g., research labs, marine parks. While these environments afford a certain amount of experimental rigor and logistical control they are fraught with limitations in external validity, impose tremendous stress on the part of the captive animals, and place burdens on populations from which they are often captured. Alternatively, over the past three decades, some researchers have sought to focus their attention on the presence of free-ranging cetacean individuals and groups who have initiated, or chosen to participate in, sociable interactions with humans in the wild. This new approach, defined as Interspecies Collaborative Research between cetacean and human, involves developing novel ways to address research questions under natural conditions and respecting the individual cetacean's autonomy. It also offers a range of potential direct benefits to the cetaceans studied, as well as allowing for unprecedented cognitive and psychological research on sociable mysticetes. Yet stringent precautions are warranted so as to not increase their vulnerability to human activities or pathogens. When conducted in its best and most responsible form, collaborative research with free-ranging cetaceans can deliver methodological innovation and invaluable new insights while not necessitating the ethical and scientific compromises that characterize research in captivity. Further, it is representative of a new epoch in science in which research is designed so that the participating cetaceans are the direct recipients of the benefits.

A claim in search of evidence: reply to Manger's thermogenesis hypothesis of cetacean brain structure.

In a recent publication in Biological Reviews, Manger (2006) made the controversial claim that the large brains of cetaceans evolved to generate heat during oceanic cooling in the Oligocene epoch and not, as is the currently accepted view, as a basis for an increase in cognitive or information-processing capabilities in response to ecological or social pressures. Manger further argued that dolphins and other cetaceans are considerably less intelligent than generally thought. In this review we challenge Manger's arguments and provide abundant evidence that modern cetacean brains are large in order to support complex cognitive abilities driven by social and ecological forces.

Volumetric neuroimaging of the atlantic white-sided dolphin (Lagenorhynchus acutus) brain from in situ magnetic resonance images.

The structure and development of the brain are extremely difficult to study in free-ranging marine mammals. Here, we report measurements of total white matter (WM), total gray matter (GM), cerebellum (WM and GM), hippocampus, and corpus callosum made from magnetic resonance (MR) images of fresh, postmortem brains of the Atlantic white-sided dolphin (Lagenorhynchus acutus) imaged in situ (i.e., the brain intact within the skull, with the head still attached to the body). WM:GM volume ratios of the entire brain increased from fetus to adult, illustrating the increase in myelination during ontogeny. The cerebellum (WM and GM combined) of subadult and adult dolphins ranged from 13.8 to 15.0% of total brain size, much larger than that of primates. The corpus callosum mid-sagittal area to brain mass ratios (CCA/BM) ranged from 0.088 to 0.137, smaller than in most mammals. Dolphin hippocampal volumes were smaller than those of carnivores, ungulates, and humans, consistent with previous qualitative results assessed from histological studies of the bottlenose dolphin brain. These quantitative measurements of white matter, gray matter, corpus callosum, and hippocampus are the first to be determined from MR images for any cetacean species. We establish here an approach for accurately determining the size of brain structures from in situ MR images of stranded, dead dolphins. This approach can be used not only for comparative and developmental studies of marine mammal brains but also for investigation of the potential impacts of natural and anthropogenic chemicals on neurodevelopment and neuroanatomy in exposed marine mammal populations.

Neuroanatomy of the subadult and fetal brain of the Atlantic white-sided dolphin (Lagenorhynchus acutus) from in situ magnetic resonance images.

This article provides the first anatomically labeled, magnetic resonance imaging (MRI) -based atlas of the subadult and fetal Atlantic white-sided dolphin (Lagenorhynchus acutus) brain. It differs from previous MRI-based atlases of cetaceans in that it was created from images of fresh, postmortem brains in situ rather than extracted, formalin-fixed brains. The in situ images displayed the classic hallmarks of odontocete brains: fore-shortened orbital lobes and pronounced temporal width. Olfactory structures were absent and auditory regions (e.g., temporal lobes and inferior colliculi) were enlarged. In the subadult and fetal postmortem MRI scans, the hippocampus was identifiable, despite the relatively small size of this structure in cetaceans. The white matter tracts of the fetal hindbrain and cerebellum were pronounced, but in the telencephalon, the white matter tracts were much less distinct, consistent with less myelin. The white matter tracts of the auditory pathways in the fetal brains were myelinated, as shown by the T2 hypointensity signals for the inferior colliculus, cochlear nuclei, and trapezoid bodies. This finding is consistent with hearing and auditory processing regions maturing in utero in L. acutus, as has been observed for most mammals. In situ MRI scanning of fresh, postmortem specimens can be used not only to study the evolution and developmental patterns of cetacean brains but also to investigate the impacts of natural toxins (such as domoic acid), anthropogenic chemicals (such as polychlorinated biphenyls, polybrominated diphenyl ethers, and their hydroxylated metabolites), biological agents (parasites), and noise on the central nervous system of marine mammal species.

Cetacean brains: how aquatic are they?

The adaptation of cetaceans to a fully aquatic lifestyle represents one of the most dramatic transformations in mammalian evolutionary history. Two of the most salient features of modern cetaceans are their fully aquatic lifestyle and their large brains. This review article will offer an overview of comparative neuroanatomical research on aquatic mammals, including analyses of odontocete cetacean, sirenian, pinniped, and fossil archaeocete brains. In particular, the question of whether a relationship exists between being fully aquatic and having a large brain is addressed. It has been hypothesized that the large, well-developed cetacean brain is a direct product of adaptation to a fully aquatic lifestyle. The current consensus is that the paleontological evidence on brain size evolution in cetaceans is not consistent with this hypothesis. Cetacean brain enlargement took place millions of years after adaptation to a fully aquatic existence. Neuroanatomical comparisons with sirenians and pinnipeds provide no evidence for the idea that the odontocete's large brain, high encephalization level, and extreme neocortical gyrification is an adaptation to a fully aquatic lifestyle. Although echolocation has been suggested as a reason for the high encephalization level in odontocetes, it should be noted that not all aquatic mammals echolocate and echolocating terrestrial mammals (e.g., bats) are not particularly highly encephalized. Echolocation is not a requirement of a fully aquatic lifestyle and, thus, cannot be considered a sole effect of aquaticism on brain enlargement. These results indicate that the high encephalization level of odontocetes is likely related to their socially complex lifestyle patterns that transcend the influence of an aquatic environment.

Large brains and lengthened life history periods in Odontocetes.

Previous work on primates and birds suggests that large brains require longer periods of juvenile growth, leading to reproductive constraints due to delayed maturation. However, longevity is often extended in large-brained species, possibly compensating for delayed maturation. We examined the relationship between brain size and life history periods in cetaceans, a large-brained mammalian order that has been largely ignored. We looked at males and females of twenty-five species of Odontocetes, using independent contrasts and multiple regressions to disentangle possible phylogenetic effects and inter-correlations among life history traits. We corrected all variables for body size allometry and separated life span into adult and juvenile periods. For females and both sexes combined, gestation, time to sexual maturity, time as an adult and life span were all positively associated with residual brain size in simple regressions; in multiple regressions, maximum life span and time as an adult were the best predictors of brain size. Males showed few significant trends. Our results suggest that brain size has co-evolved with extended life history periods in Odontocetes, as it has in primates and birds, and that a lengthened adult period could have been an important component of encephalization in cetaceans.

Cortical complexity in cetacean brains.

Cetaceans (dolphins, whales, and porpoises) have a long, dramatically divergent evolutionary history compared with terrestrial mammals. Throughout their 55-60 million years of evolution, cetaceans acquired a compelling set of characteristics that include echolocation ability (in odontocetes), complex auditory and communicative capacities, and complex social organization. Moreover, although cetaceans have not shared a common ancestor with primates for over 90 million years, they possess a set of cognitive attributes that are strikingly convergent with those of many primates, including great apes and humans. In contrast, cetaceans have evolved a highly unusual combination of neurobiological features different from that of primates. As such, cetacean brains offer a critical opportunity to address questions about how complex behavior can be based on very different neuroanatomical and neurobiological evolutionary products. Cetacean brains and primate brains are arguably most meaningfully conceived as alternative evolutionary routes to neurobiological and cognitive complexity. In this article, we summarize data on brain size and hemisphere surface configuration in several cetacean species and present an overview of the cytoarchitectural complexity of the cerebral cortex of the bottlenose dolphin.

Nature's experiments in brain diversity.

This special issue of The Anatomical Record originates from a symposium on the evolution of neurobiological specializations in mammals held at the American Association of Anatomists annual meeting in San Diego in April 2005. The symposium, co-organized by Patrick R. Hof and Lori Marino, provided the impetus for extending the discussion to a greater range of species. This special issue is the product of that goal and is fueled by the philosophy that it is largely against a backdrop of brain diversity that we can extract the higher-order commonalities across brains that may lead us to uncovering general higher-order principles of brain and behavioral evolution. Several major themes emerge from this issue. These are that there are no simple brains, that brains reflect ecology, and that brain evolution is a detective story. The 12 articles in this issue are outstanding reflections of these themes.