Brain Behavior and Evolution最新文献

Background: The origin and maintenance of species is a unifying theme in evolutionary biology. Mate choice and selection on sexual signals have emerged as powerful drivers of reproductive isolation - the key pillar of the biological species concept. The mechanistic underpinnings of isolating behaviors lie in the circuit- and cellular-level properties of the brain and remain relatively understudied.

Summary: Here, I argue that temporal auditory selectivity in anuran amphibians offers a window into the proximate mechanisms of reproductive isolation. First, I discuss anuran behaviors as a longstanding neuroethological model with which to examine behavioral reproductive isolation and its neural correlates. Next, I review how modern neurobiological techniques are revealing the proximate mechanisms of the evolution of divergent mate preferences in anurans, highlighting cellular-level neural shifts in temporal coding. Finally, I discuss future research directions to reveal the neural mechanisms through which behavioral isolation is generated and maintained in anuran model systems.

Key messages: Anurans offer a powerful model for addressing questions about how neural barriers to gene flow arise across biological scales and how changes in the brain contribute to speciation. Modern evolutionary neurobiology will benefit from applying new tools to this longstanding neuroethological model clade.

Introduction: Movement requires maneuvers that generate thrust to either make turns or move the body forward in physical space. The computational space for perpetually controlling the relative position of every point on the body surface can be vast. We hypothesize the evolution of efficient design for movement that minimizes active (neural) control by leveraging the passive (reactive) forces between the body and the surrounding medium at play. To test our hypothesis, we investigate the presence of stereotypical postures during free-swimming in adult zebrafish, Danio rerio.

Methods: We perform markerless tracking using DeepLabCut (DLC), a deep learning pose-estimation toolkit, to track geometric relationships between body parts. We identify putative clusters of postural configurations from twelve freely behaving zebrafish, using unsupervised multivariate time-series analysis (B-SOiD machine-learning software) and of distances and angles between body segments extracted from DLC data.

Results: When applied to single individuals, DLC-extracted data reveal a best-fit for 36-50 clusters in contrast to 86 clusters for data pooled from all 12 animals. The centroids of each cluster obtained over 14,000 sequential frames represent an a priori classification into relatively stable "target body postures." We use multidimensional scaling of mean parameter values for each cluster to map cluster centroids within two dimensions of postural space. From a posteriori visual analysis, we condense neighboring postural variants into 15 superclusters or core body configurations. We develop a nomenclature specifying the anteroposterior level/s (upper, mid, and lower) and degree of bending.

Conclusion: Our results suggest that constraining bends to mainly three anteroposterior levels in fish paved the way for the evolution of a neck, fore- and hind limb design for maneuverability in land vertebrates.

Introduction: Raoellidae are small artiodactyls retrieved from the middle Eocene of Asia (ca. -47 Ma) and closely related to stem Cetacea. Morphological observations of their endocranial structures allow for outlining some of the early steps of the evolutionary history of the cetacean brain. The external features of the brain and associated sinuses of Raoellidae are so far only documented by the virtual reconstruction of the endocast based on specimens of the species Indohyus indirae. These specimens are however too deformed to fully access the external morphology, surface area, and volume measurements of the brain.

Methods: We bring here new elements to the picture of the raoellid brain by an investigation of the internal structures of an exceptionally well-preserved cranium collected from the Kalakot area (Jammu and Kashmir, India) referred to the species Khirtharia inflata. Micro-CT scan investigation and virtual reconstruction of the endocast and associated sinuses of this specimen provide crucial additional data about the morphological diversity within Raoellidae as well as reliable linear, surfaces, and volumes measurements, allowing for quantitative studies.

Results: We show that, like I. indirae, the brain of K. inflata exhibits a mosaic of features observed in earliest artiodactyls: a small neocortex with simple folding pattern, widely exposed midbrain, and relatively long cerebellum. But, like Indohyus, the brain of Khirtharia shows unique derived characters also observed in stem cetaceans: narrow elongated olfactory bulbs and peduncles, posterior location of the braincase in the cranium, and complex network of blood vessels around the cerebellum. The volume of the brain relative to body mass of K. inflata is markedly small when compared to other early artiodactyls.

Conclusion: We show here that cetaceans that nowadays have the second biggest brain after humans derive from a group of animals that had a lower-than-average expected brain size. This is probably a side effect of the adaptation to aquatic life. Conversely, this very small brain size relative to body mass might be another line of evidence supporting the aquatic habits in raoellids.

Introduction: Different functional domains can be identified along the longitudinal axis of the mammalian hippocampus. We have recently hypothesized that a similar functional gradient may exist along the longitudinal axis of the avian hippocampal formation (HF) as well. If the 2 gradients are homologous, we would expect the caudal HF to be more responsive to acute stress than the rostral HF.

Methods: We restrained 8 adult Dekalb White hens in a bag for 30 min under red-light conditions and compared FOS-immunoreactive (FOS-ir) cell densities in different hippocampal subdivisions to control hens.

Results: Although we could find no evidence of an activated stress response in the hypothalamic-pituitary-adrenal axis of the restrained birds, we did find a significant increase in FOS-ir cell densities in the rostral HF of the restrained birds compared to controls.

Conclusion: We speculate that the HF response is not due to an acute stress response, but instead, it is related to the change in spatial context that was part of taking the birds and restraining them in a different room. We see no activation in the caudal HF. This would be consistent with our hypothesis that the longitudinal axis of the avian HF is homologous to the long axis of the mammalian hippocampus.

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Introduction: Pythons are a well-studied model of postprandial physiological plasticity. Consuming a meal evokes a suite of physiological changes in pythons including one of the largest documented increases in post-feeding metabolic rates relative to resting values. However, little is known about how this plasticity manifests in the brain. Previous work has shown that cell proliferation in the python brain increases 6 days following meal consumption. This study aimed to confirm these findings and build on them in the long term by tracking the survival and maturation of these newly created cells across a 2-month period.

Methods: We investigated differences in neural cell proliferation in ball pythons 6 days after a meal with immunofluorescence using the cell-birth marker 5-bromo-12'-deoxyuridine (BrdU). We investigated differences in neural cell maturation in ball pythons 2 months after a meal using double immunofluorescence for BrdU and a reptilian ortholog of the neuronal marker Fox3.

Results: We did not find significantly greater rates of cell proliferation in snakes 6 days after feeding, but we did observe more new cells in neurogenic regions in fed snakes 2 months after the meal. Feeding was not associated with higher rates of neurogenesis, but snakes that received a meal had higher numbers of newly created nonneuronal cells than fasted controls. We documented particularly high cell survival rates in the olfactory bulbs and lateral cortex.

Conclusion: Consuming a meal stimulates cell proliferation in the brains of ball pythons after digestion is complete, although this effect emerged at a later time point in this study than expected. Higher rates of proliferation partially account for greater numbers of newly created non-neuronal cells in the brains of fed snakes 2 months after the meal, but our results also suggest that feeding may have a mild neuroprotective effect. We captured a slight trend toward higher cell survival rates in fed snakes, and survival rates were particularly high in brain regions associated with olfactory perception and processing. These findings shed light on the relationship between energy balance and the creation of new neural cells in the brains of ball pythons.

Introduction: Neural exaptations represent descent via transitions to novel neural functions. A primary transition in human cognitive and neural evolution was from a predominantly socially oriented primate brain to a brain that also instantiates and subserves science, technology, and engineering, all of which depend on mathematics. Upon what neural substrates and upon what evolved cognitive mechanisms did human capacities for science, technology, engineering, and mathematics (STEM), and especially its mathematical underpinnings, emerge? Previous theory focuses on roles for tools, language, and arithmetic in the cognitive origins of STEM, but none of these factors appears sufficient to support the transition.

Methods: In this article, I describe and evaluate a novel hypothesis for the neural origins and substrates of STEM-based cognition: that they are based in human kinship systems and human maximizing of inclusive fitness.

Results: The main evidence for this hypothesis is threefold. First, as demonstrated by anthropologists, human kinship systems exhibit complex mathematical and geometrical structures that function under sets of explicit rules, and such systems and rules pervade and organize all human cultures. Second, human kinship underlies the core algebraic mechanism of evolution, maximization of inclusive fitness, quantified as personal reproduction plus the sum of all effects on reproduction of others, each multiplied by their coefficient of relatedness to self. This is the only "natural" equation expected to be represented in the human brain. Third, functional imaging studies show that kinship-related cognition activates frontal-parietal regions that are also activated in STEM-related tasks. In turn, the decision-making that integrates kinship levels with costs and benefits from alternative behaviors has recently been shown to recruit the lateral septum, a hub region that combines internal (from the prefrontal cortex, amygdala, and other regions) and external information relevant to social behavior, using a dedicated subsystem of neurons specific to kinship.

Conclusions: Taken together, these lines of evidence suggest that kinship systems and kin-associated behaviors may represent exaptations for the origin of human STEM.

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 comparative approach is a powerful way to explore the relationship between brain structure and cognitive function. Thus far, the field has been dominated by the assumption that a bigger brain somehow means better cognition. Correlations between differences in brain size or neuron number between species and differences in specific cognitive abilities exist, but these correlations are very noisy. Extreme differences exist between clades in the relationship between either brain size or neuron number and specific cognitive abilities. This means that correlations become weaker, not stronger, as the taxonomic diversity of sampled groups increases. Cognition is the outcome of neural networks. Here we propose that considering plausible neural network models will advance our understanding of the complex relationships between neuron number and different aspects of cognition. Computational modelling of networks suggests that adding pathways, or layers, or changing patterns of connectivity in a network can all have different specific consequences for cognition. Consequently, models of computational architecture can help us hypothesise how and why differences in neuron number might be related to differences in cognition. As methods in connectomics continue to improve and more structural information on animal brains becomes available, we are learning more about natural network structures in brains, and we can develop more biologically plausible models of cognitive architecture. Natural animal diversity then becomes a powerful resource to both test the assumptions of these models and explore hypotheses for how neural network structure and network size might delimit cognitive function.

Introduction: Transitions in temporal niche have occurred many times over the course of mammalian evolution. These are associated with changes in sensory stimuli available to animals, particularly with visual cues, because levels of light are so much higher during the day than at night. This relationship between temporal niche and available sensory stimuli elicits the expectation that evolutionary transitions between diurnal and nocturnal lifestyles will be accompanied by modifications of sensory systems that optimize the ability of animals to receive, process, and react to important stimuli in the environment.

Methods: This study examines the influence of temporal niche on investment in sensory brain tissue of 13 rodent species (five diurnal; eight nocturnal). Animals were euthanized and the brains immediately frozen on dry ice; olfactory bulbs were subsequently dissected and weighed, and the remaining brain was weighed, sectioned, and stained. Stereo Investigator was used to calculate volumes of four sensory regions that function in processing visual (lateral geniculate nucleus, superior colliculus) and auditory (medial geniculate nucleus, inferior colliculus) information. A phylogenetic framework was used to assess the influence of temporal niche on the relative sizes of these brain structures and of olfactory bulb weights.

Results: Compared to nocturnal species, diurnal species had larger visual regions, whereas nocturnal species had larger olfactory bulbs than their diurnal counterparts. Of the two auditory structures examined, one (medial geniculate nucleus) was larger in diurnal species, while the other (inferior colliculus) did not differ significantly with temporal niche.

Conclusion: Our results indicate a possible indirect association between temporal niche and auditory investment and suggest probable trade-offs of investment between olfactory and visual areas of the brain, with diurnal species investing more in processing visual information and nocturnal species investing more in processing olfactory information.