Evolutionary Neuroscience Research Articles

A historical perspective on the insect central complex: Anatomy, development, and function

The central complex (CX), a remarkable brain region at the core of insect behaviors, has been the subject of extensive research for decades. In this review, we offer a comprehensive historical perspective on the anatomy, development, and function of the CX. The CX consists of discrete and highly structured neuropils found at the center of the brain, which are conserved across insects and arthropods. The developmental processes that shape the CX are themselves conserved across insects. In early research, the CX had been shown to receive visual information and control motor function. Using increasingly advanced methods throughout the years, it has become clear that the CX is involved in high-level behavioral control, such as in vector navigation and goal directed orientation. Its numerical simplicity presents a rare opportunity to study structure-function relationships in small brains, gain insights into evolutionary neurobiology, and develop novel neuromorphic technologies inspired by insect brains. Since the CX is a highly conserved brain region involved in the control of spatial tasks, it is uniquely suited to gain a detailed understanding of the computations required for these processes at the level of neural circuits.

Neuronal Circuit Evolution: From Development to Structure and Adaptive Significance.

Neuronal circuits represent the functional units of the brain. Understanding how the circuits are generated to perform computations will help us understand how the brain functions. Nevertheless, neuronal circuits are not engineered, but have formed through millions of years of animal evolution. We posit that it is necessary to study neuronal circuit evolution to comprehensively understand circuit function. Here, we review our current knowledge regarding the mechanisms that underlie circuit evolution. First, we describe the possible genetic and developmental mechanisms that have contributed to circuit evolution. Then, we discuss the structural changes of circuits during evolution and how these changes affected circuit function. Finally, we try to put circuit evolution in an ecological context and assess the adaptive significance of specific examples. We argue that, thanks to the advent of new tools and technologies, evolutionary neurobiology now allows us to address questions regarding the evolution of circuitry and behavior that were unimaginable until very recently.

Economics from a biological perspective: the role of sociocultural homeostasis

ABSTRACT Economics and biology have long been overlapping and mutually enriching fields. We contribute to this cross-fertilization by spelling out the implications for economic theory of some recent insights from evolutionary neurobiology. We note that dynamic homeostasis, a core feature of life processes, has shaped social interactions at varied stages of evolution – from the patterns of competition and cooperation among early life forms to the complex process of human cultures. The resulting homeostatic perspective is not compatible with several leading economic theories but does provide a biological footing for promising concepts such as ecological rationality, heuristics, heterogeneity of economic agents, and complex, self-organizing dynamics.

Evolution of neural circuitry and cognition.

Neural circuits govern the interface between the external environment, internal cues and outwardly directed behaviours. To process multiple environmental stimuli and integrate these with internal state requires considerable neural computation. Expansion in neural network size, most readily represented by whole brain size, has historically been linked to behavioural complexity, or the predominance of cognitive behaviours. Yet, it is largely unclear which aspects of circuit variation impact variation in performance. A key question in the field of evolutionary neurobiology is therefore how neural circuits evolve to allow improved behavioural performance or innovation. We discuss this question by first exploring how volumetric changes in brain areas reflect actual neural circuit change. We explore three major axes of neural circuit evolution-replication, restructuring and reconditioning of cells and circuits-and discuss how these could relate to broader phenotypes and behavioural variation. This discussion touches on the relevant uses and limitations of volumetrics, while advocating a more circuit-based view of cognition. We then use this framework to showcase an example from the insect brain, the multi-sensory integration and internal processing that is shared between the mushroom bodies and central complex. We end by identifying future trends in this research area, which promise to advance the field of evolutionary neurobiology.

Comparative MRI analysis of the forebrain of three sauropsida models

The study of the brain by magnetic resonance imaging (MRI) allows to obtain detailed anatomical images, useful to describe specific encephalic structures and to analyze possible variabilities. It is widely used in clinical practice and is becoming increasingly used in veterinary medicine, even in exotic animals; however, despite its potential, its use in comparative neuroanatomy studies is still incipient. It is a technology that in recent years has significantly improved anatomical resolution, together with the fact that it is non-invasive and allows for systematic comparative analysis. All this makes it particularly interesting and useful in evolutionary neuroscience studies, since it allows for the analysis and comparison of brains of rare or otherwise inaccessible species. In the present study, we have analyzed the prosencephalon of three representative sauropsid species, the turtle Trachemys scripta (order Testudine), the lizard Pogona vitticeps (order Squamata) and the snake Python regius (order Squamata) by MRI. In addition, we used MRI sections to analyze the total brain volume and ventricular system of these species, employing volumetric and chemometric analyses together. The raw MRI data of the sauropsida models analyzed in the present study are available for viewing and downloading and have allowed us to produce an atlas of the forebrain of each of the species analyzed, with the main brain regions. In addition, our volumetric data showed that the three groups presented clear differences in terms of total and ventricular brain volumes, particularly the turtles, which in all cases presented distinctive characteristics compared to the lizards and snakes.

Social Brain Perspectives on the Social and Evolutionary Neuroscience of Human Language.

Human language and social cognition are two key disciplines that have traditionally been studied as separate domains. Nonetheless, an emerging view suggests an alternative perspective. Drawing on the theoretical underpinnings of the social brain hypothesis (thesis of the evolution of brain size and intelligence), the social complexity hypothesis (thesis of the evolution of communication), and empirical research from comparative animal behavior, human social behavior, language acquisition in children, social cognitive neuroscience, and the cognitive neuroscience of language, it is argued that social cognition and language are two significantly interconnected capacities of the human species. Here, evidence in support of this view reviews (1) recent developmental studies on language learning in infants and young children, pointing to the important crucial benefits associated with social stimulation for youngsters, including the quality and quantity of incoming linguistic information, dyadic infant/child-to-parent non-verbal and verbal interactions, and other important social cues integral for facilitating language learning and social bonding; (2) studies of the adult human brain, suggesting a high degree of specialization for sociolinguistic information processing, memory retrieval, and comprehension, suggesting that the function of these neural areas may connect social cognition with language and social bonding; (3) developmental deficits in language and social cognition, including autism spectrum disorder (ASD), illustrating a unique developmental profile, further linking language, social cognition, and social bonding; and (4) neural biomarkers that may help to identify early developmental disorders of language and social cognition. In effect, the social brain and social complexity hypotheses may jointly help to describe how neurotypical children and adults acquire language, why autistic children and adults exhibit simultaneous deficits in language and social cognition, and why nonhuman primates and other organisms with significant computational capacities cannot learn language. But perhaps most critically, the following article argues that this and related research will allow scientists to generate a holistic profile and deeper understanding of the healthy adult social brain while developing more innovative and effective diagnoses, prognoses, and treatments for maladies and deficits also associated with the social brain.

The evolutionary neuroscience of domestication.

How does domestication affect the brain? This question has broad relevance. Domesticated animals play important roles in human society, and substantial recent work has addressed the hypotheses that a domestication syndrome links phenotypes across species, including Homo sapiens. Surprisingly, however, neuroscience research on domestication remains largely disconnected from current knowledge about how and why brains change in evolution. This article aims to bridge that gap. Examination of recent research reveals some commonalities across species, but ultimately suggests that brain changes associated with domestication are complex and variable. We conclude that interactions between behavioral, metabolic, and life-history selection pressures, as well as the role the role of experience and environment, are currently largely overlooked and represent important directions for future research.

The evolutionary psychology of ownership is rooted in the Lockean liberal principle of self-ownership.

The psychology of ownership is rooted in self-ownership. The human brain has an evolved interoceptive sense of owning the body that supports self-ownership and the ownership of external things as extensions of the self-owning self. In this way, evolutionary neuroscience supports a Lockean liberal conception of equal natural rights rooted in natural self-ownership.

Vocal learning, chorusing seal pups, and the evolution of rhythm

The presence of vocal learning and rhythm capacities in only a few mammals drives a cross-species hypothesis in evolutionary neuroscience: vocal learning and rhythm perception and synchronization may be causally related. Harbor seals (Phoca vitulina) are among these mammals, and their puppyhood is the most active vocal period in their lives. Building on both comparative psychology and animal behavior, this research integrates methods from human cognition with attention to species’ ecological sensory niches. We present data from seal pups in four different setups: recordings of semi-natural vocal interactions in (1) individual and (2) group settings, (3) playback experiments to elicit vocal responses, and (4) perceptual listening experiments to measure behavioral responses. We complement empirical data with agent-based computational modeling aimed at reverse-engineering the putative mechanisms underlying rhythmic vocal interactions. Our data suggest that seal pups have developed capacities to produce and perceive rhythmic patterns. Seals’ vocal exchanges show rhythmic interactivity and antisynchronous coordination. Evidence for antisynchrony, rather than synchrony, in seals suggests that the rhythm-vocal learning link across species is more complex than previously surmised.

Two distinct evolutionary conserved neural degeneration pathways characterized in a colonial chordate

Colonial tunicates are marine organisms that possess multiple brains simultaneously during their colonial phase. While the cyclical processes of neurogenesis and neurodegeneration characterizing their life cycle have been documented previously, the cellular and molecular changes associated with such processes and their relationship with variation in brain morphology and individual (zooid) behavior throughout adult life remains unknown. Here, we introduce Botryllus schlosseri as an invertebrate model for neurogenesis, neural degeneration, and evolutionary neuroscience. Our analysis reveals that during the weekly colony budding (i.e., asexual reproduction), prior to programmed cell death and removal by phagocytes, decreases in the number of neurons in the adult brain are associated with reduced behavioral response and significant change in the expression of 73 mammalian homologous genes associated with neurodegenerative disease. Similarly, when comparing young colonies (1 to 2 y of age) to those reared in a laboratory for ∼20 y, we found that older colonies contained significantly fewer neurons and exhibited reduced behavioral response alongside changes in the expression of 148 such genes (35 of which were differentially expressed across both timescales). The existence of two distinct yet apparently related neurodegenerative pathways represents a novel platform to study the gene products governing the relationship between aging, neural regeneration and degeneration, and loss of nervous system function. Indeed, as a member of an evolutionary clade considered to be a sister group of vertebrates, this organism may be a fundamental resource in understanding how evolution has shaped these processes across phylogeny and obtaining mechanistic insight.

Multilevel atlas comparisons reveal divergent evolution of the primate brain

Whether the size of the prefrontal cortex (PFC) in humans is disproportionate when compared to other species is a persistent debate in evolutionary neuroscience. This question has left the study of over/under-expansion in other structures relatively unexplored. We therefore sought to address this gap by adapting anatomical areas from the digital atlases of 18 mammalian species, to create a common interspecies classification. Our approach used data-driven analysis based on phylogenetic generalized least squares to evaluate anatomical expansion covering the whole brain. Our main finding suggests a divergence in primate evolution, orienting the stereotypical mammalian cerebral proportion toward a frontal and parietal lobe expansion in catarrhini (primate parvorder comprising old world monkeys, apes, and humans). Cerebral lobe volumes slopes plotted for catarrhini species were ranked as parietal∼frontal > temporal > occipital, contrasting with the ranking of other mammalian species (occipital > temporal > frontal∼parietal). Frontal and parietal slopes were statistically different in catarrhini when compared to other species through bootstrap analysis. Within the catarrhini's frontal lobe, the prefrontal cortex was the principal driver of frontal expansion. Across all species, expansion of the frontal lobe appeared to be systematically linked to the parietal lobe. Our findings suggest that the human frontal and parietal lobes are not disproportionately enlarged when compared to other catarrhini. Nevertheless, humans remain unique in carrying the most relatively enlarged frontal and parietal lobes in an infraorder exhibiting a disproportionate expansion of these areas.

Statistical Atlases and Automatic Labeling Strategies to Accelerate the Analysis of Social Insect Brain Evolution

Current methods used to quantify brain size and compartmental scaling relationships in studies of social insect brain evolution involve manual annotations of images from histological samples, confocal microscopy or other sources. This process is susceptible to human bias and error and requires time-consuming effort by expert annotators. Standardized brain atlases, constructed through 3D registration and automatic segmentation, surmount these issues while increasing throughput to robustly sample diverse morphological and behavioral phenotypes. Here we design and evaluate three strategies to construct statistical brain atlases, or templates, using ants as a model taxon. The first technique creates a template by registering multiple brains of the same species. Brain regions are manually annotated on the template, and the labels are transformed back to each individual brain to obtain an automatic annotation, or to any other brain aligned with the template. The second strategy also creates a template from multiple brain images but obtains labels as a consensus from multiple manual annotations of individual brains comprising the template. The third technique is based on a template comprising brains from multiple species and the consensus of their labels. We used volume similarity as a metric to evaluate the automatic segmentation produced by each method against the inter- and intra-individual variability of human expert annotators. We found that automatic and manual methods are equivalent in volume accuracy, making the template technique an extraordinary tool to accelerate data collection and reduce human bias in the study of the evolutionary neurobiology of ants and other insects.

Socioecology and Evolutionary Neurobiology of Predatory Ants

OPINION article Front. Ecol. Evol., 15 February 2022 | https://doi.org/10.3389/fevo.2021.804200

A Smaller Habenula is Associated with Increasing Intensity of Sexual Selection

The habenula is a small structure in the brain that acts as a relay station for neural information, helping to modulate behaviour in response to variable and unpredictable stimuli. Broadly, it is evolutionarily conserved in structure and connectivity across vertebrates and is the most prominent bilaterally asymmetric structure in the brain. Nonetheless, comparative evolutionary studies of the habenula are virtually non-existent. Here, we examine the volumes of the medial and lateral habenular subregions, in both hemispheres, across a group of Australian agamid lizards in the genus Ctenophorus. In males, we found bilaterally asymmetrical selection on the lateral habenula to become smaller with increasing intensity of sexual selection, possibly as a mechanism to increase aggressive responses. In females, we found bilaterally symmetrical selection on both the medial and lateral subregions to become smaller with increasing sexual selection. This is consistent with sexual selection increasing motivation to reproduce and the habenula’s well-characterized role in controlling and modifying responses to rewarding stimuli. However, as there are currently no studies addressing habenular function in reptiles, it is difficult to draw more precise conclusions. As has happened recently in biomedical neuroscience, it is time for the habenula to receive greater attention in evolutionary neuroscience.

“And Binding with Briars, my Joys and Desires”: Discussion of Janine de Peyer’s “Unspoken Rhapsody”

This paper discusses Janine de Peyer’s “Unspoken Rhapsody: Female Erotic Countertransference and the Dissociation of Desire,” elaborating on the professional and clinical aspects of working with female erotic countertransference with male patients, with a focus on dissociation and containment in these contexts. Perspectives from evolutionary psychology and affective neuroscience are offered to better understand how female analyst/male patient dyads differ from that of male analyst/female patient.

Amphibian behavioral diversity offers insights into evolutionary neurobiology.

Recent studies have served to emphasize the unique placement of amphibians, composed of more than 8000 species, in the evolution of the brain. We provide an overview of the three amphibian orders and their respective ecologies, behaviors, and brain anatomy. Studies have probed the origins of independently evolved parental care strategies in frogs and the biophysical principles driving species-specific differences in courtship vocalization patterns. Amphibians are also important models for studying the central control of movement, especially in the context of the vertebrate origin of limb-based locomotion. By highlighting the versatility of amphibians, we hope to see a further adoption of anurans, urodeles, and gymnophionans as model systems for the evolution and neural basis of behavior across vertebrates.

Sex/Gender Attribution: When the Penis Makes the Difference

The present study aimed to replicate Kessler and McKenna’s (1978) ethnomethodological study that investigated how an individual attributes gender to a person. By administering figures depicted on overlays (Overlay Study), Kessler and McKenna found that the penis more than the vulva and the male sexual characteristics more than the female ones were significantly more salient in the gender attribution process. From all this, their adage is: “See someone as female only when you cannot see them as male.” Taking as a model Kessler and McKenna’s Overlay Study, we administered to 592 adults 120 new digital stimuli elaborated on realistic frontal images of human nudes to verify if the previously obtained results would be confirmed by using more realistic images. We found that the participants attributed male gender 86% of the time when the penis was shown, but only attributed female gender 67% of the time when the vulva was shown. All findings had strong statistical significance, confirming the findings of the Overlay Study that the penis makes the difference in gender recognition. Beyond an ethnomethodological approach, we have interpreted and discussed our results from the outlook of evolutionary and cognitive psychology and cognitive neuroscience, concluding that the cultural stereotypes and prejudices that affect gender attribution might not just be a mere cultural product, but rather the consequence of evolved cognitive biases.

A genetically tractable jellyfish model for systems and evolutionary neuroscience

Jellyfish are radially symmetric organisms without a brain that arose more than 500 million years ago. They achieve organismal behaviors through coordinated interactions between autonomously functioning body parts. Jellyfish neurons have been studied electrophysiologically, but not at the systems level. We introduce Clytia hemisphaerica as a transparent, genetically tractable jellyfish model for systems and evolutionary neuroscience. Wegenerate stable F1 transgenic lines for cell-type-specific conditional ablation and whole-organism GCaMP imaging. Using these tools and computational analyses, we find that an apparently diffusenetwork of RFamide-expressing umbrellar neurons is functionally subdivided into a series of spatially localized subassemblies whose synchronous activation controls directional food transfer from the tentacles to the mouth. These data reveal anunanticipated degree of structured neural organization in this species. Clytia affords a platform for systems-level studies of neural function, behavior, and evolution within a clade of marine organisms with growing ecological and economic importance.

Generation of knock-in lampreys by CRISPR-Cas9-mediated genome engineering

The lamprey represents the oldest group of living vertebrates and has been a key organism in various research fields such as evolutionary developmental biology and neuroscience. However, no knock-in technique for this animal has been established yet, preventing application of advanced genetic techniques. Here, we report efficient generation of F0 knock-in lampreys by CRISPR-Cas9-mediated genome editing. A donor plasmid containing a heat-shock promoter was co-injected with a short guide RNA (sgRNA) for genome digestion, a sgRNA for donor plasmid digestion, and Cas9 mRNA. Targeting different genetic loci, we succeeded in generating knock-in lampreys expressing photoconvertible protein Dendra2 as well as those expressing EGFP. With its simplicity, design flexibility, and high efficiency, we propose that the present method has great versatility for various experimental uses in lamprey research and that it can also be applied to other “non-model” organisms.

Morphological characteristics of the forebrain in the donkey (Equus asinus): A compared atlas of magnetic resonance imaging and cross-sectional anatomy.

The brain is the most essential part of the central nervous system which regulates and coordinates all body activities. Based on its phylogenetic development from the neural tube, the brain is divided into rhombencephalon (hindbrain), mesencephalon (midbrain) and prosencephalon (forebrain). The present study is achieved to describe the morphological characteristics of the normal forebrain in the donkey using the matched magnetic resonance imaging (MRI) and cross-sectional anatomy. Ten cadaveric heads of healthy adult donkeys of both sexes were used. Two heads were examined using a 1.5Tesla MRI scanner, and the brains of the other heads were gently extracted; six brains were sectioned into transverse, dorsal and sagittal slices, and two brains were grossly inspected. MR images were selected in correlation to their closely corresponding gross sections. Both cross-sectional anatomy and MRI scans showed extensive gyration of the neocortex. The forebrain structures appeared with variable intensities on three sequences, Flair, T1-weighted and T2-weighted MRI, enabling comprehensive evaluation of the relevant neuroanatomical structures. The present study provided a precise neuroanatomical atlas of the forebrain in the donkey which could help in the quick and efficient interpretation of clinical diseases of the forebrain, localization of the forebrain functions and evolutionary neurobiology.