Structural connectivity of the multiple demand network in humans and comparison to the macaque brain.

Fluid intelligence encompasses a wide range of abilities such as working memory, problem-solving, and relational reasoning. In the human brain, these abilities are associated with the Multiple Demand Network, traditionally thought to involve combined activity of specific regions predominantly in the prefrontal and parietal cortices. However, the structural basis of the interactions between areas in the Multiple Demand Network, as well as their evolutionary basis among primates, remains largely unexplored. Here, we exploit diffusion MRI to elucidate the major white matter pathways connecting areas of the human core and extended Multiple Demand Network. We then investigate whether similar pathways can be identified in the putative homologous areas of the Multiple Demand Network in the macaque monkey. Finally, we contrast human and monkey networks using a recently proposed approach to compare different species' brains within a common organizational space. Our results indicate that the core Multiple Demand Network relies mostly on dorsal longitudinal connections and, although present in the macaque, these connections are more pronounced in the human brain. The extended Multiple Demand Network relies on distinct pathways and communicates with the core Multiple Demand Network through connections that also appear enhanced in the human compared with the macaque.

Ocular Necessities: A Neuroethological Perspective on Vertebrate Visual Development.

BACKGROUND: By examining species-specific innate behaviours, neuroethologists have characterized unique neural strategies and specializations from throughout the animal kingdom. Simultaneously, the field of evolutionary developmental biology (informally, "evo-devo") seeks to make inferences about animals' evolutionary histories through careful comparison of developmental processes between species, because evolution is the evolution of development. Yet despite the shared focus on cross-species comparisons, there is surprisingly little crosstalk between these two fields. Insights can be gleaned at the intersection of neuroethology and evo-devo. Every animal develops within an environment, wherein ecological pressures advantage some behaviours and disadvantage others. These pressures are reflected in the neurodevelopmental strategies employed by different animals across taxa. SUMMARY: Vision is a system of particular interest for studying the adaptation of animals to their environments. The visual system enables a wide variety of animals across the vertebrate lineage to interact with their environments, presenting a fantastic opportunity to examine how ecological pressures have shaped animals' behaviours and developmental strategies. Applying a neuroethological lens to the study of visual development, we advance a novel theory that accounts for the evolution of spontaneous retinal waves, an important phenomenon in the development of the visual system, across the vertebrate lineage. KEY MESSAGES: We synthesize literature on spontaneous retinal waves from across the vertebrate lineage. We find that ethological considerations explain some cross-species differences in the dynamics of retinal waves. In zebrafish, retinal waves may be more important for the development of the retina itself, rather than the retinofugal projections. We additionally suggest empirical tests to determine whether Xenopus laevis experiences retinal waves.

The Japan Monkey Centre Primates Brain Imaging Repository of high-resolution postmortem magnetic resonance imaging: The second phase of the archive of digital records.

A comparison of neuroanatomical features of the brain between humans and our evolutionary relatives, nonhuman primates, is key to understanding the human brain system and the neural basis of mental and neurological disorders. Although most comparative MRI studies of human and nonhuman primate brains have been based on brains of primates that had been used as subjects in experiments, it is essential to investigate various species of nonhuman primates in order to elucidate and interpret the diversity of neuroanatomy features among humans and nonhuman primates. To develop a research platform for this purpose, it is necessary to harmonize the scientific contributions of studies with the standards of animal ethics, animal welfare, and the conservation of brain information for long-term continuation of the field. In previous research, we first developed a gated data-repository of anatomical images obtained using 9.4-T ex vivo MRI of postmortem brain samples from 12 nonhuman primate species, and which are stored at the Japan Monkey Centre. In the present study, as a second phase, we released a collection of T2-weighted images and diffusion tensor images obtained in nine species: white-throated capuchin, Bolivian squirrel monkey, stump-tailed macaque, Tibet monkey, Sykes' monkey, Assamese macaque, pig-tailed macaque, crested macaque, and chimpanzee. Our image repository should facilitate scientific discoveries in the field of comparative neuroscience. This repository can also promote animal ethics and animal welfare in experiments with nonhuman primate models by optimizing methods for in vivo and ex vivo MRI scanning of brains and supporting veterinary neuroradiological education. In addition, the repository is expected to contribute to conservation, preserving information about the brains of various primates, including endangered species, in a permanent digital form.

Comparative Brain Imaging Reveals Analogous and Divergent Patterns of Species and Face Sensitivity in Humans and Dogs.

Conspecific-preference in social perception is evident for multiple sensory modalities and in many species. There is also a dedicated neural network for face processing in primates. However, the evolutionary origin and the relative role of neural species sensitivity and face sensitivity in visuo-social processing are largely unknown. In this comparative study, species sensitivity and face sensitivity to identical visual stimuli (videos of human and dog faces and occiputs) were examined using functional magnetic resonance imaging in dogs (n = 20; 45% female) and humans (n = 30; 50% female). In dogs, the bilateral mid suprasylvian gyrus showed conspecific-preference, no regions exhibited face-preference, and the majority of the visually-responsive cortex showed greater conspecific-preference than face-preference. In humans, conspecific-preferring regions (the right amygdala/hippocampus and the posterior superior temporal sulcus) also showed face-preference, and much of the visually-responsive cortex showed greater face-preference than conspecific-preference. Multivariate pattern analyses (MVPAs) identified species-sensitive regions in both species, but face-sensitive regions only in humans. Across-species representational similarity analyses (RSAs) revealed stronger correspondence between dog and human response patterns for distinguishing conspecific from heterospecific faces than other contrasts. Results unveil functional analogies in dog and human visuo-social processing of conspecificity but suggest that cortical specialization for face perception may not be ubiquitous across mammals.SIGNIFICANCE STATEMENT To explore the evolutionary origins of human face-preference and its relationship to conspecific-preference, we conducted the first comparative and noninvasive visual neuroimaging study of a non-primate and a primate species, dogs and humans. Conspecific-preferring brain regions were observed in both species, but face-preferring brain regions were observed only in humans. In dogs, an overwhelming majority of visually-responsive cortex exhibited greater conspecific-preference than face-preference, whereas in humans, much of the visually-responsive cortex showed greater face-preference than conspecific-preference. Together, these findings unveil functional analogies and differences in the organizing principles of visuo-social processing across two phylogenetically distant mammal species.

Adaptation to stimulus orientation in mouse primary visual cortex.

Information processing in the visual system is shaped by recent stimulus history, such that prolonged viewing of an adapting stimulus can alter the perception of subsequently presented test stimuli. In the tilt-after-effect, the perceived orientation of a grating is often repelled away from the orientation of a previously viewed adapting grating. A possible neural correlate for the tilt-after-effect has been described in cat and macaque primary visual cortex (V1), where adaptation produces repulsive shifts in the orientation tuning curves of V1 neurons. We investigated adaptation to stimulus orientation in mouse V1 to determine whether known species differences in orientation processing, notably V1 functional architecture and proportion of tightly tuned cells, are important for these repulsive shifts. Unlike the consistent repulsion reported in other species, we found that repulsion was only about twice as common as attraction in our mouse data. Furthermore, adapted responses were attenuated across all orientations. A simple model that captured key physiological findings reported in cats and mice indicated that the greater proportion of broadly tuned neurons in mice may explain the observed species differences in adaptation.

Mini-review: Wild laughs: Ontogenesis and phylogenesis of humour.

This mini-review discusses the existing evidence on various forms of humour and humour-like behaviour in non-human animals, combining ontogenetic and phylogenetic perspectives. The first section describes humour-like behaviours, from the simplest to the most complex form (from laughing, tickling, joking, and chasing to ToM humour). In the second section, we propose the SPeCies (Social, Physiological, and Cognitive) Perspective, which frames the various types of humour based on Social motivation, Physiological state, and Cognitive skills. Finally, in the third section, we discuss future directions for further development.

Common and distinct neural mechanisms of attention.

Despite a constant deluge of sensory stimulation, only a fraction of it is used to guide behavior. This selective processing is generally referred to as attention, and much research has focused on the neural mechanisms controlling it. Recently, research has broadened to include more ways by which different species selectively process sensory information, whether due to the sensory input itself or to different behavioral and brain states. This work has produced a complex and disjointed body of evidence across different species and forms of attention. However, it has also provided opportunities to better understand the breadth of attentional mechanisms. Here, we summarize the evidence that suggests that different forms of selective processing are supported by mechanisms both common and distinct.

Let's talk about sex: Mechanisms of neural sexual differentiation in Bilateria.

In multicellular organisms, sexed gonads have evolved that facilitate release of sperm versus eggs, and bilaterian animals purposefully combine their gametes via mating behaviors. Distinct neural circuits have evolved that control these physically different mating events for animals producing eggs from ovaries versus sperm from testis. In this review, we will describe the developmental mechanisms that sexually differentiate neural circuits across three major clades of bilaterian animals-Ecdysozoa, Deuterosomia, and Lophotrochozoa. While many of the mechanisms inducing somatic and neuronal sex differentiation across these diverse organisms are clade-specific rather than evolutionarily conserved, we develop a common framework for considering the developmental logic of these events and the types of neuronal differences that produce sex-differentiated behaviors. This article is categorized under: Congenital Diseases > Stem Cells and Development Neurological Diseases > Stem Cells and Development.

The brain of the silver fox (Vulpes vulpes): a neuroanatomical reference of cell-stained histological and MRI images.

Although the silver fox (Vulpes vulpes) has been largely overlooked by neuroscientists, it has the potential to serve as a powerful model for the investigation of brain-behavior relationships. The silver fox is a melanistic variant of the red fox. Within this species, the long-running Russian farm-fox experiment has resulted in different strains bred to show divergent behavior. Strains bred for tameness, aggression, or without selection on behavior present an excellent opportunity to investigate neuroanatomical changes underlying behavioral characteristics. Here, we present a histological and MRI neuroanatomical reference of a fox from the conventional strain, which is bred without behavioral selection. This can provide an anatomical basis for future studies of the brains of foxes from this particular experiment, as well as contribute to an understanding of fox brains in general. In addition, this can serve as a resource for comparative neuroscience and investigations into neuroanatomical variation among the family Canidae, the order Carnivora, and mammals more broadly.

The evolution of social timing.

Sociality and timing are tightly interrelated in human interaction as seen in turn-taking or synchronised dance movements. Sociality and timing also show in communicative acts of other species that might be pleasurable, but also necessary for survival. Sociality and timing often co-occur, but their shared phylogenetic trajectory is unknown: How, when, and why did they become so tightly linked? Answering these questions is complicated by several constraints; these include the use of divergent operational definitions across fields and species, the focus on diverse mechanistic explanations (e.g., physiological, neural, or cognitive), and the frequent adoption of anthropocentric theories and methodologies in comparative research. These limitations hinder the development of an integrative framework on the evolutionary trajectory of social timing and make comparative studies not as fruitful as they could be. Here, we outline a theoretical and empirical framework to test contrasting hypotheses on the evolution of social timing with species-appropriate paradigms and consistent definitions. To facilitate future research, we introduce an initial set of representative species and empirical hypotheses. The proposed framework aims at building and contrasting evolutionary trees of social timing toward and beyond the crucial branch represented by our own lineage. Given the integration of cross-species and quantitative approaches, this research line might lead to an integrated empirical-theoretical paradigm and, as a long-term goal, explain why humans are such socially coordinated animals.

Beyond language: The unspoken sensory-motor representation of the tongue in non-primates, non-human and human primates.

The English idiom "on the tip of my tongue" commonly acknowledges that something is known, but it cannot be immediately brought to mind. This phrase accurately describes sensorimotor functions of the tongue, which are fundamental for many tongue-related behaviors (e.g., speech), but often neglected by scientific research. Here, we review a wide range of studies conducted on non-primates, non-human and human primates with the aim of providing a comprehensive description of the cortical representation of the tongue's somatosensory inputs and motor outputs across different phylogenetic domains. First, we summarize how the properties of passive non-noxious mechanical stimuli are encoded in the putative somatosensory tongue area, which has a conserved location in the ventral portion of the somatosensory cortex across mammals. Second, we review how complex self-generated actions involving the tongue are represented in more anterior regions of the putative somato-motor tongue area. Finally, we describe multisensory response properties of the primate and non-primate tongue area by also defining how the cytoarchitecture of this area is affected by experience and deafferentation.

Cell types and molecular architecture of the Octopus bimaculoides visual system.

Cephalopods have a remarkable visual system, with a camera-type eye and high acuity vision that they use for a wide range of sophisticated visually driven behaviors. However, the cephalopod brain is organized dramatically differently from that of vertebrates and invertebrates, and beyond neuroanatomical descriptions, little is known regarding the cell types and molecular determinants of their visual system organization. Here, we present a comprehensive single-cell molecular atlas of the octopus optic lobe, which is the primary visual processing structure in the cephalopod brain. We combined single-cell RNA sequencing with RNA fluorescence in situ hybridization to both identify putative molecular cell types and determine their anatomical and spatial organization within the optic lobe. Our results reveal six major neuronal cell classes identified by neurotransmitter/neuropeptide usage, in addition to non-neuronal and immature neuronal populations. We find that additional markers divide these neuronal classes into subtypes with distinct anatomical localizations, revealing further diversity and a detailed laminar organization within the optic lobe. We also delineate the immature neurons within this continuously growing tissue into subtypes defined by evolutionarily conserved developmental genes as well as novel cephalopod- and octopus-specific genes. Together, these findings outline the organizational logic of the octopus visual system, based on functional determinants, laminar identity, and developmental markers/pathways. The resulting atlas presented here details the "parts list" for neural circuits used for vision in octopus, providing a platform for investigations into the development and function of the octopus visual system as well as the evolution of visual processing.

Of mice and monkeys: Somatosensory processing in two prominent animal models.

Our understanding of the neural basis of somatosensation is based largely on studies of the whisker system of mice and rats and the hands of macaque monkeys. Results across these animal models are often interpreted as providing direct insight into human somatosensation. Work on these systems has proceeded in parallel, capitalizing on the strengths of each model, but has rarely been considered as a whole. This lack of integration promotes a piecemeal understanding of somatosensation. Here, we examine the functions and morphologies of whiskers of mice and rats, the hands of macaque monkeys, and the somatosensory neuraxes of these three species. We then discuss how somatosensory information is encoded in their respective nervous systems, highlighting similarities and differences. We reflect on the limitations of these models of human somatosensation and consider key gaps in our understanding of the neural basis of somatosensation.

The Neuroscience Community Has a Role in Environmental Conservation.

We previously argued that the neuroscience community has a role in environmental conservation because protection of biodiversity and the specialized behavioral adaptions of animals is essential to understanding brain structure and function. Preserving biodiversity and the natural world is also linked to human mental health and broadens our insight on the origins of psychiatric disorders like stress, anxiety, and depression. The study of neuroscience has become a global scientific pursuit that involves thousands of researchers and has an economic impact in the billions of dollars. As a group of biomedical research scientists, neuroscientists have the knowledge base and public credibility to convincingly promote sustainable environmental actions and policies. Here, we outline several key areas in which we as a neuroscience academic community can participate to preserve a rich global biodiversity and confront the environmental crises that lie before us.

Where is Cingulate Cortex? A Cross-Species View.

To compare findings across species, neuroscience relies on cross-species homologies, particularly in terms of brain areas. For cingulate cortex, a structure implicated in behavioural adaptation and control, a homologous definition across mammals is available - but currently not employed by most rodent researchers. The standard partitioning of rodent cingulate cortex is inconsistent with that in any other model species, including humans. Reviewing the existing literature, we show that the homologous definition better aligns results of rodent studies with those of other species, and reveals a clearer structural and functional organisation within rodent cingulate cortex itself. Based on these insights, we call for widespread adoption of the homologous nomenclature, and reinterpretation of previous studies originally based on the nonhomologous partitioning of rodent cingulate cortex.

Large-scale comparative neuroimaging: Where are we and what do we need?

Neuroimaging has a lot to offer comparative neuroscience. Although invasive "gold standard" techniques have a better spatial resolution, neuroimaging allows fast, whole-brain, repeatable, and multi-modal measurements of structure and function in living animals and post-mortem tissue. In the past years, comparative neuroimaging has increased in popularity. However, we argue that its most significant potential lies in its ability to collect large-scale datasets of many species to investigate principles of variability in brain organisation across whole orders of species-an ambition that is presently unfulfilled but achievable. We briefly review the current state of the field and explore what the current obstacles to such an approach are. We propose some calls to action.

Aging is associated with larger brain mass and volume in homing pigeons (Columba livia).

In mammals, the brain decreases in mass and volume as a function of age. The current study is, to the best of our knowledge, the first to investigate age-related changes in brain mass and volume in birds. Following perfusion, brains from young and old homing pigeons were weighed on a balance and orthogonal measurements of the telencephalon, cerebellum, and tecta were obtained with a digital caliper. It was found that older pigeons had heavier brains than younger pigeons, a difference that remained after controlling for body mass. Additionally, older pigeons had on average greater estimated telencephalon volumes than younger pigeons, again also after controlling for body mass. Cerebellum and right tectum volumes also differed between age groups after controlling for body mass, with older pigeons having a larger cerebellum and right tectum than younger pigeons. In sum, brains are on average heavier and larger in old pigeons, which display age-related cognitive decline, compared to young adult pigeons. The larger brain in older homing pigeons also lies in stark contrast with aging of the mammalian brain.

Acoustic prepulse inhibition in male and female prairie voles: Implications for models of neuropsychiatric illness.

Sensory gating, the ability to suppress sensory information of irrelevant stimuli, is affected in several neuropsychiatric diseases, notably schizophrenia and autism. It is currently unclear how these deficits interact with other hallmark symptoms of these disorders, such as social withdrawal and difficulty with interpersonal relationships. The highly affiliative prairie vole (Microtus ochrogaster) may be an ideal model organism to study the neurobiology underlying social behavior. In this study, we assessed unimodal acoustic sensory gating in male and female prairie voles using the prepulse inhibition (PPI) paradigm, whereby a lower amplitude sound (prepulse) decreases the startle response to a high amplitude sound (pulse) compared to the high amplitude sound alone. Prairie voles showed evidence of PPI at all prepulse levels compared to pulse alone, with both males and females showing similar levels of inhibition. However, unlike what has been reported in other rodent species, prairie voles did not show a within-session decrease in startle response to the pulse alone, nor did they show a decrease in startle response to the pulse over multiple days, highlighting their inability to habituate to startling stimuli (short- and long-term). When contrasted with a cohort of male wildtype C57Bl/6J mice that underwent a comparable PPI protocol, individual voles showed significantly higher trial-by-trial variability as well as longer latency to startle than mice. The benefits and caveats to using prairie voles in future sensory gating experiments are discussed.

Large-scale temporo-parieto-frontal networks for motor and cognitive motor functions in the primate brain.

The extent to which neural circuits and mechanisms underlying sensory, motor, and cognitive cortical functions in the human brain are shared with those of other animals, especially non-human primates, is currently a key issue in the field of comparative neuroscience. Cortical functions result from the conjoint function of different, reciprocally connected areas working together as large-scale functionally specialized networks, which can be investigated in human subjects thanks to the development of non-invasive functional and connectional imaging techniques. In spite of their limitations in terms of spatial and temporal resolution, these techniques make it possible to address the issue of how and to what extent the neural mechanisms for different cortical functions differ from those of non-human primates. Indeed, 30 million years of independent evolution have resulted in significant differences between the brains of humans and macaques, which are the experimental model system phylogenetically closest to humans for obtaining highly detailed anatomical and functional information on the organization of cortical networks. In the macaque brain, architectonic, connectional, and functional data have provided evidence for functionally specialized large-scale cortical networks involving temporal, parietal, and frontal areas. These networks appear to play a primary role in controlling different aspects of motor and cognitive motor functions, such as hand action organization and recognition, or oculomotor behavior and gaze processing. In the present review, based on the comparison of these data with data from human studies, we will argue that there is clear evidence for human counterparts of these networks. These human and macaque putatively homolog networks appear to share phylogenetically older neural mechanisms, which, in the evolution of the human lineage, could have been exploited and differentiated, resulting in the emergence of human-specific higher-order cognitive functions. These considerations are fully in line with the notion of "neural reuse" in primate evolution.

Neural processes of vocal social perception: Dog-human comparative fMRI studies.

In this review we focus on the exciting new opportunities in comparative neuroscience to study neural processes of vocal social perception by comparing dog and human neural activity using fMRI methods. The dog is a relatively new addition to this research area; however, it has a large potential to become a standard species in such investigations. Although there has been great interest in the emergence of human language abilities, in case of fMRI methods, most research to date focused on homologue comparisons within Primates. By belonging to a very different clade of mammalian evolution, dogs could give such research agendas a more general mammalian foundation. In addition, broadening the scope of investigations into vocal communication in general can also deepen our understanding of human vocal skills. Being selected for and living in an anthropogenic environment, research with dogs may also be informative about the way in which human non-linguistic and linguistic signals are represented in a mammalian brain without skills for language production.