Brain Behavior and Evolution最新文献

The plainfin midshipman fish (Porichthys notatus) relies on the production and reception of social acoustic signals for reproductive success. During spawning, male midshipman produce long duration advertisement calls to attract females, which use their auditory sense to locate and access calling males. While seasonal changes based on reproductive state in inner-ear auditory sensitivity and frequency encoding in midshipman is well documented, little is known about reproductive-state dependent changes in central auditory sensitivity and auditory neural responsiveness to conspecific advertisement calls. Previous research indicates that forebrain dopaminergic neurons are preferentially active in response to conspecific advertisement calls and during female auditory-driven behavior in the breeding season. These dopamine neurons project to both the inner ear and central auditory nuclei and contribute to regulation of inner-ear auditory sensitivity based on reproductive state. The present study tested the hypothesis that exposure to the male advertisement call would elicit differential activation in auditory brain nuclei and in the forebrain auditory-projecting dopaminergic nucleus in reproductive vs. non-reproductive male midshipman. Fish were collected during the spring reproductive and winter non-reproductive months and were exposed to a playback of the advertisement call or ambient noise (control). Immunohistochemistry identified activated neurons (pS6-ir; proxy for neural activation) in midbrain and forebrain auditory and dopaminergic nuclei. Our results revealed that in key auditory and dopaminergic areas, the greatest activation (most pS6-ir cells) occurred in reproductive males exposed to the advertisement call.

Prairie voles (Microtus ochrogaster) are one of the few mammalian species that are monogamous and engage in the biparental rearing of their offspring. Biparental care impacts the quantity and quality of care the offspring receives. The increased attention by the father may translate to heightened tactile contact the offspring receives through licking and grooming. In the current study, we used electrophysiological multiunit recording techniques to define the organization of the perioral representation in the primary somatosensory area (S1) of prairie voles. Functional representations were related to myeloarchitectonic boundaries. Our results show that most of S1 is occupied by the representation of the contralateral mystacial whiskers and the lower and upper lips. The mystacial vibrissae representation encompassed a large portion of the caudolateral S1, while the representation of the lower and upper lips occupied a large portion of the rostrolateral aspect of S1. We found that neuronal populations representing the perioral structures tended to have small receptive fields relative to other body part representations on the head. The representation of the mystacial whiskers and perioral structures was coextensive with cytoarchitectonically defined barrel fields that extend from the caudolateral to a rostrolateral aspect of S1. We discuss our findings in the context of the magnification of behaviorally relevant sensory surfaces in other rodents, the ubiquity of the barrel systems in rodents, and behaviors associated with specialized sensory surfaces.

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.

Background: Glia represent a major cell population of the nervous system, and they take part in virtually any process sustaining the development, the functioning, and the pathology of the nervous system. Glial cells diversified significantly during evolution and distinct signals have been adopted to initiate glial development in mammals as compared to flies. In the invertebrate model Drosophila melanogaster, the transcription factor Gcm is necessary and sufficient to generate glial cells. Although Gcm orthologs have been found in protostomes and deuterostomes, they do not act in glial fate commitment as in flies, calling for further investigations of the evolutionarily conserved role of Gcm.

Summary: Here, we review the impact of the fly Gcm transcription factor in the differentiation of phagocytic competent cells inside and outside the nervous system, glia, and macrophages, respectively. Then, we discuss the evolutionary conservation of Gcm and the neural/nonneural functions of Gcm orthologs. Finally, we present a recent work from Pavlidaki et al. [Cell Rep. 2022;41(3):111506] showing that the Gcm cascade is conserved from fly macrophages to mammalian microglia to counteract acute and chronic inflammation.

Key messages: Gcm has an ancestral role in immunity, and its anti-inflammatory effect is evolutionarily conserved. This opens new avenues to assess Gcm function in other species/animal models, its potential involvement in inflammation-related processes, such as regeneration, and to expand the investigation on glia evolution.

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.

Background: Most studies comparing forebrain organization between reptiles and mammals have focused on similarities. Equally important are the differences between their brains. While differences have been addressed infrequently, this approach can highlight the evolution of brains in relation to their respective environments.

Summary: This review focuses on three key differences between the dorsal and ventral thalamus of reptiles and mammals. One is the organization of thalamo-telencephalic interconnections. Reptiles have at least three circuits that transmit information between the dorsal thalamus and telencephalon, whereas mammals have just one. A second is the number and distribution of local circuit neurons in the dorsal thalamus. Most reptilian dorsal thalamic nuclei lack local circuit neurons, whereas these same nuclei in mammals contain varying numbers. The third is the organization of the thalamic reticular nucleus. In crocodiles, at least, the neurons in the thalamic reticular nucleus are heterogeneous with two separate nuclei each being associated with a different circuit. In mammals, the neurons in the thalamic reticular nucleus, which is a single structure, are homogeneous.

Key messages: Transcriptomics and development are suggested to be the most likely approaches to explain these differences between reptiles and mammals. Transcriptomics can reveal which neuron types are "new" or "old" and whether neurons and their respective circuits have been re-purposed to be used differently. Examination of the development and connections of the dorsal and ventral thalamus will determine whether their formation is similar or different from what has been described for mammals.

Introduction: To reproduce, the parasitoid emerald jewel wasp (Ampulex compressa) envenomates an American cockroach (Periplaneta americana) and barricades it in a hole with an egg on the host's leg. The larval wasp feeds externally before entering the host and consuming internal organs before forming a cocoon inside the host carcass.

Methods: The vulnerability of jewel wasp larvae to predation by juvenile cockroaches was investigated, and data were recorded with time-lapse videography.

Results: Cockroaches were found to be predators of parasitized hosts. When parasitized cockroaches were exposed to hungry cockroaches on days 0-8 of development, the developing larva was killed. Eggs were dislodged or consumed, larvae on the leg were eaten, and larvae inside the host were eaten along with the host. On day 9, 80% of the wasp larvae were killed and eaten along with the host. Conversely, on day 10, 90% of the larvae survived. On developmental day 11 or later, the wasp larva always survived, although the host carcass was consumed. Survival depended entirely on whether the cocoon had been completed.

Conclusion: The results highlight the vulnerability of larvae to predation and suggest the cocoon defends from insect mandibles. This may explain the unusual feeding behavior of the jewel wasp larvae, which eat the host with remarkable speed, tapping into the host respiratory system in the process, and consuming vital organs early, in contrast to many other parasitoids. Results are discussed in relation to larval wasp behavior, evolution, and development, and potential predators are considered.

Background: The evolution of the primate brain has been characterized by the reorganization of key structures and circuits underlying derived specializations in sensory systems, as well as social behavior and cognition. Among these, expansion and elaboration of the prefrontal cortex has been accompanied by alterations to the connectivity and organization of subcortical structures, including the striatum and amygdala, underlying advanced aspects of executive function, inhibitory behavioral control, and socioemotional cognition seen in our lineages. At the cellular level, the primate brain has further seen an increase in the diversity and number of inhibitory GABAergic interneurons. A prevailing hypothesis holds that disruptions in the balance of excitatory to inhibitory activity in the brain underlies the pathophysiology of many neurodevelopmental and psychiatric disorders.

Summary: This review highlights the evolution of inhibitory brain systems and circuits and suggests that recent evolutionary modifications to GABAergic circuitry may provide the substrate for vulnerability to aberrant neurodevelopment. We further discuss how modifications to primate and human social organization and life history may shape brain development in ways that contribute to neurodivergence and the origins of neurodevelopmental disorders.

Key messages: Many brain systems have seen functional reorganization in the mammalian, primate, and human brain. Alterations to inhibitory circuitry in frontostriatal and frontoamygdalar systems support changes in social behavior and cognition. Increased complexity of inhibitory systems may underlie vulnerabilities to neurodevelopmental and psychiatric disorders, including autism and schizophrenia. Changes observed in Williams syndrome may further elucidate the mechanisms by which alterations in inhibitory systems lead to changes in behavior and cognition. Developmental processes, including altered neuroimmune function and age-related vulnerability of inhibitory cells and synapses, may lead to worsening symptomatology in neurodevelopmental and psychiatric disorders.