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A cerebellar substrate for cognition evolved multiple times independently in mammals
Abstract and Figures
ELife digest
The brains of mammals consist of the same basic structures, but each of these structures varies from one species to the next. A given structure may be larger in one species than another, for example. It may contain different numbers or sizes of cells. It may even have different connections to other brain regions. By comparing individual brain structures between species, we can map how the mammalian brain has evolved.
Smaers et al. have now done this for the cerebellum, a structure at the back of the brain. The mammalian cerebellum consists of three main areas: the vermis, paravermis, and the lateral hemispheres. Smaers et al. show that in apes, dolphins and seals, the lateral hemispheres are unusually large relative to the cerebellum as a whole. This could indicate that these three groups of animals share a common ancestor with enlarged lateral hemispheres. Yet, genetic studies suggest that this is not the case.
Another possibility is that apes, dolphins and seals independently evolved enlarged lateral hemispheres. This may have given rise to a trait that proved beneficial for each of them. But what might this be? Studies in people suggest that the lateral hemispheres help to support some forms of learning. Apes, dolphins and seals are among only a few species of mammal with the ability to learn new calls and vocalizations. The expansion of the lateral cerebellum may therefore have contributed to the evolution of vocal learning, and this may have occurred independently on at least three separate occasions.
Future work should extend this analysis to other cognitive skills, as well as to other species. Bats, for example, would be of particular interest because of their ability to echolocate. Finally, the lateral hemispheres consist of several subregions that play different roles in learning and information processing. Further experiments should explore whether different subregions have increased in size in different species.
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Supplementary resources (4)
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... Mammals from four orders showed the same coordinated scaling of neuron number in both the cerebral and cerebellar cortices, supporting arguments for integrated functions and selective pressures [88]. Indeed, some researchers argue that the cerebellum has been neglected in studies of vertebrate brain evolution and cognition [89][90][91]. ...
... Thus, one constraint on an individual's quantitative cognition is the biological capacity for information processing in their brain, as determined genetically and developmentally for each species [74][75][76][77][78][79][80][81]. Additionally, quantitative precision was related to neuron density in the cerebellum, a brain structure that has been overlooked in studies of vertebrate brain evolution and cognition [89][90][91]. We found that density of neurons was a more accurate proxy for quantitative ability than brain volume when comparing species across taxa. ...
The ability to represent approximate quantities appears to be phylogenetically widespread, but the selective pressures and proximate mechanisms favouring this ability remain unknown. We analysed quantity discrimination data from 672 subjects across 33 bird and mammal species, using a novel Bayesian model that combined phylogenetic regression with a model of number psychophysics and random effect components. This allowed us to combine data from 49 studies and calculate the Weber fraction (a measure of quantity representation precision) for each species. We then examined which cognitive, socioecological and biological factors were related to variance in Weber fraction. We found contributions of phylogeny to quantity discrimination performance across taxa. Of the neural, socioecological and general cognitive factors we tested, cortical neuron density and domain-general cognition were the strongest predictors of Weber fraction, controlling for phylogeny. Our study is a new demonstration of evolutionary constraints on cognition, as well as of a relation between species-specific neuron density and a particular cognitive ability.
This article is part of the theme issue ‘Systems neuroscience through the lens of evolutionary theory’.
... Alongside this, the cerebellum is thought to be important in social intelligence [1], particularly in terms of the links between sensory-motor control and social interactions and understanding [85,86]. Indeed, it is now thought the expansion of the cortico-cerebellar system is the primary driver of brain expansion in anthropoid primates [87], suggesting the increased behavioural complexity in mammals could be partly explained by selection on the cerebellum [88]. So much so, that Fernandes et al., [89] found residual cerebellar size to be the most appropriate proxy when compared to a measure of general intelligence; as cerebellar models produced the most similar model fit results when compared to those produced using a measure of general intelligence. ...
... Considerable attention has been paid to primate brain evolution (e.g., [14,20,90,91]), perhaps the result of the anthropocentricism and since there are substantial data available on this taxonomic group making comparative tests easy to implement. Likewise, carnivorans are also now receiving attention (e.g., [19,88,92,93]) since variation in their brain and body size, and ranging social and physical environments, makes them excellent models for these tests too. Indeed, most of the literature surrounding brain size hypotheses is based on analyses of these two groups. ...
Despite decades of research, much uncertainty remains regarding the selection pressures responsible for brain size variation. Whilst the influential social brain hypothesis once garnered extensive support, more recent studies have failed to find support for a link between brain size and sociality. Instead, it appears there is now substantial evidence suggesting ecology better predicts brain size in both primates and carnivores. Here, different models of brain evolution were tested, and the relative importance of social, ecological, and life-history traits were assessed on both overall encephalisation and specific brain regions. In primates, evidence is found for consistent associations between brain size and ecological factors, particularly diet; however, evidence was also found advocating sociality as a selection pressure driving brain size. In carnivores, evidence suggests ecological variables, most notably home range size, are influencing brain size; whereas, no support is found for the social brain hypothesis, perhaps reflecting the fact sociality appears to be limited to a select few taxa. Life-history associations reveal complex selection mechanisms to be counterbalancing the costs associated with expensive brain tissue through extended developmental periods, reduced fertility, and extended maximum lifespan. Future studies should give careful consideration of the methods chosen for measuring brain size, investigate both whole brain and specific brain regions where possible, and look to integrate multiple variables, thus fully capturing all of the potential factors influencing brain size.
... The finding that cerebellar neurons account for most of the difference in neuron numbers between reptiles and endotherms is interesting in light of the mounting evidence that the cerebellum plays a key role in the evolution of sensorimotor and cognitive control of complex behaviors (38)(39)(40)(41). ...
Significance
The evolution of brain processing capacity has traditionally been inferred from data on brain size. However, similarly sized brains of distantly related species can differ in the number and distribution of neurons, their basic computational units. Therefore, a finer-grained approach is needed to reveal the evolutionary paths to increased cognitive capacity. Using a new, comprehensive dataset, we analyzed brain cellular composition across amniotes. Compared to reptiles, mammals and birds have dramatically increased neuron numbers in the telencephalon and cerebellum, which are brain parts associated with higher cognition. Astoundingly, a phylogenetic analysis suggests that as few as four major changes in neuron–brain scaling in over 300 million years of evolution pave the way to intelligence in endothermic land vertebrates.
... Although the cerebellum in most cetaceans and in elephants is much larger in both relative and absolute size compared to other eutherians (Marino et al. 2000;Maseko et al. 2012), the neuronal morphology of the elephant and cetacean cerebellum is very consistent with what has been observed in other mammals (Jacobs et al. 2014), and likely responds to impoverishment in a similar manner. The disproportionate size of the cerebellum in elephants and cetaceans, particularly in the lateral hemispheres (Smaers et al. 2018), appears to be related to its sensory acquisition and processing role and the importance of infrasound in elephants and echolocation in cetaceans for exploring the environment (Hanson et al. 2013;Jacobs et al. 2014). It remains unclear to what extent the cerebellum also contributes to cognitive and emotional functions in elephants and cetaceans, although such functions have been demonstrated in other species (primates: Habas 2021; rats: Shipman and Green 2020). ...
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.
... Lastly, the elephant's cerebellum has deviated markedly in evolution. It is the relatively largest compared to the rest of the brain size of all other mammals, and the lateral cerebellar hemispheres are expanded compared to the vermis (Maseko et al., 2012), although there are mammals that have greater lateral cerebellar relative enlargement (Smaers et al., 2018). The elephant cerebellum is specialized such that it has increased neurons relative to the cerebral cortex [97.5% of the 257 billion neurons in the elephant brain are found in the cerebellum (Herculano-Houzel et al., 2014)], and the neurons are packed more compactly than in other afrotherians (Herculano-Houzel et al., 2014). ...
Elephants are large-brained, social mammals with a long lifespan. Studies of elephants can provide insight into the aging process, which may be relevant to understanding diseases that affect elderly humans because of their shared characteristics that have arisen through independent evolution. Elephants become sexually mature at 12 to 14 years of age and are known to live into, and past, their 7 th decade of life. Because of their relatively long lifespans, elephants may have evolved mechanisms to counter age-associated morbidities, such as cancer and cognitive decline. Elephants rely heavily on their memory, and engage in multiple levels of competitive and collaborative relationships because they live in a fission-fusion system. Female matrilineal relatives and dependent offspring form tight family units led by an older-aged matriarch, who serves as the primary repository for social and ecological knowledge in the herd. Similar to humans, elephants demonstrate a dependence on social bonds, memory, and cognition to navigate their environment, behaviors that might be associated with specializations of brain anatomy. Compared with other mammals, the elephant hippocampus is proportionally smaller, whereas the temporal lobe is disproportionately large and expands laterally. The elephant cerebellum is also relatively enlarged, and the cerebral cortex is highly convoluted with numerous gyral folds, more than in humans. Last, an interesting characteristic unique to elephants is the presence of at least 20 copies of the TP53 tumor suppressor gene . Humans have only a single copy. TP53 encodes for the p53 protein, which is known to orchestrate cellular response to DNA damage. The effects of these multiple copies of TP53 are still being investigated, but it may be to protect elephants against multiple age-related diseases. For these reasons, among others, studies of elephants would be highly informative for aging research. Elephants present an underappreciated opportunity to explore further common principles of aging in a large-brained mammal with extended longevity. Such research can contribute to contextualizing our knowledge of age-associated morbidities in humans.
Epigenetic age has emerged as an important biomarker of biological aging. It has revealed that some tissues age faster than others, which is vital to understanding the complex phenomenon of aging and developing effective interventions. Previous studies have demonstrated that humans exhibit heterogeneity in pace of epigenetic aging among brain structures that are consistent with differences in structural and microanatomical deterioration. Here, we add comparative data on epigenetic brain aging for chimpanzees, humans' closest relatives. Such comparisons can further our understanding of which aspects of human aging are evolutionarily conserved or specific to our species, especially given that humans are distinguished by a long lifespan, large brain, and, potentially, more severe neurodegeneration with age. Specifically, we investigated epigenetic aging of the dorsolateral prefrontal cortex and cerebellum, of humans and chimpanzees by generating genome-wide CpG methylation data and applying established epigenetic clock algorithms to produce estimates of biological age for these tissues. We found that both species exhibit relatively slow epigenetic aging in the brain relative to blood. Between brain structures, humans show a faster rate of epigenetic aging in the dorsolateral prefrontal cortex compared to the cerebellum, which is consistent with previous findings. Chimpanzees, in contrast, show comparable rates of epigenetic aging in the two brain structures. Greater epigenetic change in the human dorsolateral prefrontal cortex compared to the cerebellum may reflect both the protracted development of this structure in humans and its greater age-related vulnerability to neurodegenerative pathology.
Human brains are exceptionally large, support distinctive cognitive processes, and evolved by natural selection to mediate adaptive behavior. Comparative biology situates the human brain within an evolutionary context to illuminate how it has been shaped by selection and how its structure relates to evolutionary function, while identifying the developmental and molecular changes that were involved. Recent applications of powerful phylogenetic methods have uncovered new findings, some of which overturn conventional wisdom about how and why brains evolve. Here, we focus on four long-standing claims about brain evolution and discuss how new work has either contradicted these claims or shown the relevant phenomena to be more complicated than previously appreciated. Throughout, we emphasize studies of non-human primates and hominins, our close relatives and recent ancestors.
Using tyrosine hydroxylase immunohistochemistry, we describe the nuclear parcellation of the catecholaminergic system in the brains of a lar gibbon (Hylobates lar) and a chimpanzee (Pan troglodytes). The parcellation of catecholaminergic nuclei in the brains of both apes is virtually identical to that observed in humans and shows very strong similarities to that observed in mammals more generally, particularly other primates. Specific variations of this system in the apes studied include an unusual high‐density cluster of A10dc neurons, an enlarged retrorubral nucleus (A8), and an expanded distribution of the neurons forming the dorsolateral division of the locus coeruleus (A4). The additional A10dc neurons may improve dopaminergic modulation of the extended amygdala, the enlarged A8 nucleus may be related to the increased use of communicative facial expressions in the hominoids compared to other primates, while the expansion of the A4 nucleus appears to be related to accelerated evolution of the cerebellum in the hominoids compared to other primates. In addition, we report the presence of a compact division of the locus coeruleus proper (A6c), as seen in other primates, that is not present in other mammals apart from megachiropteran bats. The presence of this nucleus in primates and megachiropteran bats may reflect homology or homoplasy, depending on the evolutionary scenario adopted. The fact that the complement of homologous catecholaminergic nuclei are mostly consistent across mammals, including primates, is advantageous for the selection of model animals for the study of specific dysfunctions of the catecholaminergic system in humans. This article is protected by copyright. All rights reserved.
Interpretations have been made of a currently narrow range of signal types that humans can record from interstellar sources, to determine if distant life forms exist. This chapter briefly surveys the types of signals now available and what they and others could reveal about distant life forms in the future. The chapter then explores the assessment of intelligent species if they visit Earth. The authors ask which observable signs could indicate self‐awareness and ethical thinking, and how humans can test for the presence of ethics. A “Goldilocks Evolutionary Sequence” of neurocognitive features is presented, which can be operationalized as a plan to vet interstellar visitors and a protocol for negotiating with them. Important distinctions may point toward ethics, but if a visit to Earth occurs, will humans have the time to make them?
The themes that arise as we enter the philosophical discussion on astrobiology are many and diverse. Of all these, ethics is presented as a rather complex one. Therefore, astrobioethics is the branch of philosophy and astrobiology that is responsible for studying the moral implications of the search for life in space. In this chapter I will analyze three fundamental aspects: epistemological, astrotheological, and interplanetary issues. Each has its own field of discussion and questions that need to be addressed, so that our new small step for mankind does not end up crushing the life we find in the universe.
Comparative studies tend to differ from optimality and functionality studies in how they treat adaptation. While the comparative approach focuses on the origin and change of traits, optimality studies assume that adaptations are maintained at an optimum by stabilizing selection. This paper presents a model of adaptive evolution on a macroevolutionary time scale that includes the maintenance of traits at adaptive optima by stabilizing selection as the dominant evolutionary force. Interspecific variation is treated as variation in the position of adaptive optima. The model illustrates how phylogenetic constraints not only lead to correlations between phylogenetically related species, but also to imperfect adaptations. From this model, a statistical comparative method is derived that can be used to estimate the effect of a selective factor on adaptive optima in a way that would be consistent with an optimality study of adaptation to this factor. The method is illustrated with an analysis of dental evolution in fossil horses. The use of comparative methods to study evolutionary trends is also discussed.
The large brain and small postcanine teeth of modern humans are among our most distinctive features, and trends in their evolution are well studied within the hominin clade. Classic accounts hypothesize that larger brains and smaller teeth coevolved because behavioral changes associated with increased brain size allowed a subsequent dental reduction. However, recent studies have found mismatches between trends in brain enlargement and posterior tooth size reduction in some hominin species. We use a multiple-variance Brownian motion approach in association with evolutionary simulations to measure the tempo and mode of the evolution of endocranial and dental size and shape within the hominin clade. We show that hominin postcanine teeth have evolved at a relatively consistent neutral rate, whereas brain size evolved at comparatively more heterogeneous rates that cannot be explained by a neutral model, with rapid pulses in the branches leading to later Homo species. Brain reorganization shows evidence of elevated rates only much later in hominin evolution, suggesting that fast-evolving traits such as the acquisition of a globular shape may be the result of direct or indirect selection for functional or structural traits typical of modern humans.
Understanding the biological foundations of language is vital to gaining insight into how the capacity for language may have evolved in humans. Animal models can be exploited to learn about the biological underpinnings of shared human traits, and although no other animals display speech or language, a range of behaviors found throughout the animal kingdom are relevant to speech and spoken language. To date, such investigations have been dominated by studies of our closest primate relatives searching for shared traits, or more distantly related species that are sophisticated vocal communicators, like songbirds. Herein I make the case for turning our attention to the Chiropterans, to shed new light on the biological encoding and evolution of human language-relevant traits. Bats employ complex vocalizations to facilitate navigation as well as social interactions, and are exquisitely tuned to acoustic information. Furthermore, bats display behaviors such as vocal learning and vocal turn-taking that are directly pertinent for human spoken language. Emerging technologies are now allowing the study of bat vocal communication, from the behavioral to the neurobiological and molecular level. Although it is clear that no single animal model can reflect the complexity of human language, by comparing such findings across diverse species we can identify the shared biological mechanisms likely to have influenced the evolution of human language.
Research on the evolution of human speech and music benefits from hypotheses and data generated in a number of disciplines. The purpose of this article is to illustrate the high relevance of pinniped research for the study of speech, musical rhythm, and their origins, bridging and complementing current research on primates and birds. We briefly discuss speech, vocal learning, and rhythm from an evolutionary and comparative perspective. We review the current state of the art on pinniped communication and behavior relevant to the evolution of human speech and music, showing interesting parallels to hypotheses on rhythmic behavior in early hominids. We suggest future research directions in terms of species to test and empirical data needed.
The present study focuses on the relationship between neocortical structures and functional aspects in three selected mammalian species. Our aim was to compare cortical layering and neuron density in the projection areas (somatomotor, M1; somatosensory, S1; auditory, A1; and visual, V1; each in a wider sense). Morphological and design-based stereological analysis was performed in the wild boar (Sus scrofa scrofa) as a representative terrestrial hoofed animal (artiodactyl) and the common dolphin (Delphinus delphis) as a highly derived related aquatic mammal (cetartiodactyl). For comparison, we included the human (Homo sapiens) as a well-documented anthropoid primate. In the cortex of many mammals, layer IV (inner granular layer) is the main target of specific thalamocortical inputs while layers III and V are the main origins of neocortical projections. Because the fourth layer is indistinct or mostly lacking in the primary neocortex of the wild boar and dolphins, respectively, we analyzed the adjacent layers III and V in these animals. In the human, all the three layers were investigated separately. The stereological data show comparatively low neuron densities in all areas of the wild boar and high cell counts in the human (as expected), particularly in the primary visual cortex. The common dolphin, in general, holds an intermediate position in terms of neuron density but exhibits higher values than the human in a few layers. With respect to the situation in the wild boar, stereological neuron counts in the dolphin are consistently higher, with a maximum in layer III of the visual cortex. The extended auditory neocortical field in dolphins and the hypertrophic auditory pathway indicate secondary neurobiological adaptations to their aquatic habitat during evolution. The wild boar, however, an omnivorous quadruped terrestrial mammal, shows striking specializations as to the sensorimotor neurobiology of the snout region.
In a recent contribution, Griffin & Yapuncich (2016) (‘G&Y’) report on purported inaccuracies and lack of theoretical underpinnings of our recently proposed ancestral estimation procedure. Our method is designed to provide a good overall fit with the data when different branches may be subject to different rates of change (multiple variance Brownian motion, or ‘mvBM’). Here we demonstrate that G&Y’s theoretical concerns stem from a misinformed account of basic statistical concepts and procedures, a misinterpretation of the primary literature and a circular adherence to a restrictive model of evolution (standard Brownian motion, or ‘standard BM’) whose usefulness has long been considered inappropriate for modelling branch-specific evolutionary patterns. We further apply a series of simple tests that falsify G&Y’s claims on every account. Finally, we show that including a range of sample sizes (from 4 through 100) to G&Y’s own suggested simulation procedure further substantiates what they purport to falsify: the validity of mvBM when modelling potential deviations from standard BM in trait evolution.
(Current Biology 27, 714–720; March 6, 2017) In this article, we unintentionally omitted to expand on a citation of previously published results. In the caption of Figure 2, we stated that “F and p values indicate the significance of a phylogenetic ANCOVA testing for intercept differences between humans and other primates (see also Smaers and Rohlf [9], Supplemental Information…, and Table S2 for more detailed results)” (p. 716). We would like to clarify that in this statement, “see also Smaers and Rohlf” refers, specifically and exclusively, to the phylogenetic ANCOVA of primate prefrontal cortex to primary visual cortex and frontal motor areas using the Smaers dataset in [9]. These results were depicted in a subsection of our Figure 2 (the two top left regression plots) and were numerically presented in a subsection of our Table S2. Smaers and Rohlf presented these results as an empirical example when describing the least-squares solution of phylogenetic ANCOVA and did not discuss the wider biological implications of these results for primate brain evolution. The presentation of the previous results was discussed openly during the review process of this manuscript. The authors apologize for any confusion this oversight may have caused.
Over the past 30 years, cumulative evidence has indicated that cerebellar function extends beyond sensorimotor control. This view has emerged from studies of neuroanatomy, neuroimaging, neuropsychology, and brain stimulation, with the results implicating the cerebellum in domains as diverse as attention, language, executive function, and social cognition. Although the literature provides sophisticated models of how the cerebellum helps refine movements, it remains unclear how the core mechanisms of these models can be applied when considering a broader conceptualization of cerebellar function. In light of recent multidisciplinary findings, we examine how two key concepts that have been suggested as general computational principles of cerebellar function- prediction and error-based learning- might be relevant in the operation of cognitive cerebro-cerebellar loops.
The northern elephant seal (Mirounga angustirostris) and California sea lion (Zalophus californianus) are members of a diverse clade of carnivorous mammals known as pinnipeds. Pinnipeds are notable for their large, ape-sized brains, yet little is known about their central nervous system. Both the northern elephant seal and California sea lion spend most of their lives at sea, but each also spends time on land to breed and give birth. These unique coastal niches may be reflected in specific evolutionary adaptations to their sensory systems. Here we report on components of the visual pathway in these two species. We found evidence for two classes of myelinated fibers within the pinniped optic nerve, those with thick myelin sheaths (elephant seal: 9%, sea lion: 7%) and thin myelin sheaths (elephant seal: 91%, sea lion: 93%). In order to investigate the architecture of the lateral geniculate nucleus, superior colliculus, and primary visual cortex, we processed brain sections from seal and sea lion pups for Nissl substance, cytochrome oxidase and vesicular glutamate transporters. As in other carnivores, the dorsal lateral geniculate nucleus consisted of three main layers, A, A1, and C, while each superior colliculus similarly consisted of seven distinct layers. The sea lion visual cortex is located at the posterior side of cortex between the upper and lower banks of the postlateral sulcus, while the elephant seal visual cortex extends far more anteriorly along the dorsal surface and medial wall. These results are relevant to comparative studies related to the evolution of large brains. This article is protected by copyright. All rights reserved.
One of the enduring questions that has driven neuroscientific enquiry in the last century has been the nature of differences in the prefrontal cortex of humans versus other animals [1]. The prefrontal cortex has drawn particular interest due to its role in a range of evolutionarily specialized cognitive capacities such as language [2], imagination [3], and complex decision making [4]. Both cytoarchitectonic [5] and comparative neuroimaging [6] studies have converged on the conclusion that the proportion of prefrontal cortex in the human brain is greatly increased relative to that of other primates. However, considering the tremendous overall expansion of the neocortex in human evolution, it has proven difficult to ascertain whether this extent of prefrontal enlargement follows general allometric growth patterns, or whether it is exceptional [1]. Species' adherence to a common allometric relationship suggests conservation through phenotypic integration, while species' deviations point toward the occurrence of shifts in genetic and/or developmental mechanisms. Here we investigate prefrontal cortex scaling across anthropoid primates and find that great ape and human prefrontal cortex expansion are non-allometrically derived features of cortical organization. This result aligns with evidence for a developmental heterochronic shift in human prefrontal growth [7, 8], suggesting an association between neurodevelopmental changes and cortical organization on a macroevolutionary scale. The evolutionary origin of non-allometric prefrontal enlargement is estimated to lie at the root of great apes (∼19-15 mya), indicating that selection for changes in executive cognitive functions characterized both great ape and human cortical organization.