Natural sensory context drives diverse brain-wide activity during C. elegans mating.

Natural goal-directed behaviors often involve complex sequences of many stimulus-triggered components. Understanding how brain circuits organize such behaviors requires mapping the interactions between an animal, its environment, and its nervous system. Here, we use brain-wide neuronal imaging to study the full performance of mating by the C. elegans male. We show that as mating unfolds in a sequence of component behaviors, the brain operates similarly between instances of each component but distinctly between different components. When the full sensory and behavioral context is taken into account, unique roles emerge for each neuron. Functional correlations between neurons are not fixed but change with behavioral dynamics. From individual neurons to circuits, our study shows how diverse brain-wide dynamics emerge from the integration of sensory perception and motor actions in their natural context.

Molecular Basis of Chemotactile Sensation in Octopus.

Animals display wide-ranging evolutionary adaptations based on their ecological niche. Octopuses explore the seafloor with their flexible arms using a specialized "taste by touch" system to locally sense and respond to prey-derived chemicals and movement. How the peripherally distributed octopus nervous system mediates relatively autonomous arm behavior is unknown. Here, we report that octopus arms use a family of cephalopod-specific chemotactile receptors (CRs) to detect poorly soluble natural products, thereby defining a form of contact-dependent, aquatic chemosensation. CRs form discrete ion channel complexes that mediate the detection of diverse stimuli and transduction of specific ionic signals. Furthermore, distinct chemo- and mechanosensory cells exhibit specific receptor expression and electrical activities to support peripheral information coding and complex chemotactile behaviors. These findings demonstrate that the peripherally distributed octopus nervous system is a key site for signal processing and highlight how molecular and anatomical features synergistically evolve to suit an animal's environmental context.

Neural Control of Naturalistic Behavior Choices.

In the natural world, animals make decisions on an ongoing basis, continuously selecting which action to undertake next. In the lab, however, the neural bases of decision processes have mostly been studied using artificial trial structures. New experimental tools based on the genetic toolkit of model organisms now make it experimentally feasible to monitor and manipulate neural activity in small subsets of neurons during naturalistic behaviors. We thus propose a new approach to investigating decision processes, termed reverse neuroethology. In this approach, experimenters select animal models based on experimental accessibility and then utilize cutting-edge tools such as connectomes and genetically encoded reagents to analyze the flow of information through an animal's nervous system during naturalistic choice behaviors. We describe how the reverse neuroethology strategy has been applied to understand the neural underpinnings of innate, rapid decision making, with a focus on defensive behavioral choices in the vinegar fly Drosophila melanogaster.

Mixed Selectivity Coding of Content-Temporal Detail by Dorsomedial Posterior Parietal Neurons.

The dorsomedial posterior parietal cortex (dmPPC) is part of a higher-cognition network implicated in elaborate processes underpinning memory formation, recollection, episode reconstruction, and temporal information processing. Neural coding for complex episodic processing is however under-documented. Here, we recorded extracellular neural activities from three male rhesus macaques (Macaca mulatta) and revealed a set of neural codes of "neuroethogram" in the primate parietal cortex. Analyzing neural responses in macaque dmPPC to naturalistic videos, we discovered several groups of neurons that are sensitive to different categories of ethogram items, low-level sensory features, and saccadic eye movement. We also discovered that the processing of category and feature information by these neurons is sustained by the accumulation of temporal information over a long timescale of up to 30 s, corroborating its reported long temporal receptive windows. We performed an additional behavioral experiment with additional two male rhesus macaques and found that saccade-related activities could not account for the mixed neuronal responses elicited by the video stimuli. We further observed monkeys' scan paths and gaze consistency are modulated by video content. Taken altogether, these neural findings explain how dmPPC weaves fabrics of ongoing experiences together in real time. The high dimensionality of neural representations should motivate us to shift the focus of attention from pure selectivity neurons to mixed selectivity neurons, especially in increasingly complex naturalistic task designs.

A perspective on neuroethology: what the past teaches us about the future of neuroethology.

For 100 years, the Journal of Comparative Physiology-A has significantly supported research in the field of neuroethology. The celebration of the journal's centennial is a great time point to appreciate the recent progress in neuroethology and to discuss possible avenues of the field. Animal behavior is the main source of inspiration for neuroethologists. This is illustrated by the huge diversity of investigated behaviors and species. To explain behavior at a mechanistic level, neuroethologists combine neuroscientific approaches with sophisticated behavioral analysis. The rapid technological progress in neuroscience makes neuroethology a highly dynamic and exciting field of research. To summarize the recent scientific progress in neuroethology, I went through all abstracts of the last six International Congresses for Neuroethology (ICNs 2010-2022) and categorized them based on the sensory modalities, experimental model species, and research topics. This highlights the diversity of neuroethology and gives us a perspective on the field's scientific future. At the end, I highlight three research topics that may, among others, influence the future of neuroethology. I hope that sharing my roots may inspire other scientists to follow neuroethological approaches.

Centennial issue.

The Journal of Comparative Physiology A, also known as JCPA, was founded by Karl von Frisch and Alfred Kühn in 1924, then under its German title Zeitschrift für vergleichende Physiologie. During the 100 years of its history, it became the leading international journal in comparative physiology and its daughter discipline, neuroethology. As such, it had a major impact on the development of these disciplines. In celebration of this achievement and the nearly 10,000 articles that appeared during the last 100 years, this Centennial Issue is published. Its authors reflect on the history of JCPA and the early pioneers, including women scientists, of comparative physiology; share the impact that the Journal had on their careers; discuss the benefit of the enormous taxonomic diversity of model systems used in studies published in JCPA; contrast this philosophy with the strategy of a limited number of standard biomedical model systems; review popular and trending research topics covered in JCPA; and, by interrogating the past, take a peek into the future of neuroethology.

Fantastic beasts and how to study them: rethinking experimental animal behavior.

Humans have been trying to understand animal behavior at least since recorded history. Recent rapid development of new technologies has allowed us to make significant progress in understanding the physiological and molecular mechanisms underlying behavior, a key goal of neuroethology. However, there is a tradeoff when studying animal behavior and its underlying biological mechanisms: common behavior protocols in the laboratory are designed to be replicable and controlled, but they often fail to encompass the variability and breadth of natural behavior. This Commentary proposes a framework of 10 key questions that aim to guide researchers in incorporating a rich natural context into their experimental design or in choosing a new animal study system. The 10 questions cover overarching experimental considerations that can provide a template for interspecies comparisons, enable us to develop studies in new model organisms and unlock new experiments in our quest to understand behavior.

Neural mechanisms of mutualistic fish cleaning behaviour: a study in the wild.

One crucial interaction for the health of fish communities in coral reefs is performed by cleaner fish by removing ectoparasites from the body of other fish, so-called clients. Studying the underlying mechanisms of this behaviour is essential to understanding how species react to social stimuli and defining the drivers of mutualistic social behaviour. Here, we pinpoint the neural molecular mechanisms in the cleaning behaviour of Labroides dimidiatus in the wild through an in situ interaction experiment at a coral reef in New Caledonia. Five cleaners and clients (Abudefduf saxatilis) were placed into underwater aquaria to interact, while five were not presented with a client. The brain transcriptomes revealed 233 differentially expressed genes in cleaners that were interacting with a client. Among these genes, grin2d, npy, slc6a3 and immediate early genes (IEGs; fosb and fosl1) were related to learning and memory, glutamate and dopamine pathways, which confirm molecular pathways observed in laboratory studies. However, a new potential mechanism was found with npy (neuropeptide Y) as a driver of feeding behaviour. These results show the role of neurotransmitters and IEGs in mutualistic social behaviour, unveiling the mechanism behind the feeding stimulus that leads the cleaner fish to establish mutualistic interactions in coral reefs.

Deep learning approaches for seizure video analysis: A review.

Seizure events can manifest as transient disruptions in the control of movements which may be organized in distinct behavioral sequences, accompanied or not by other observable features such as altered facial expressions. The analysis of these clinical signs, referred to as semiology, is subject to observer variations when specialists evaluate video-recorded events in the clinical setting. To enhance the accuracy and consistency of evaluations, computer-aided video analysis of seizures has emerged as a natural avenue. In the field of medical applications, deep learning and computer vision approaches have driven substantial advancements. Historically, these approaches have been used for disease detection, classification, and prediction using diagnostic data; however, there has been limited exploration of their application in evaluating video-based motion detection in the clinical epileptology setting. While vision-based technologies do not aim to replace clinical expertise, they can significantly contribute to medical decision-making and patient care by providing quantitative evidence and decision support. Behavior monitoring tools offer several advantages such as providing objective information, detecting challenging-to-observe events, reducing documentation efforts, and extending assessment capabilities to areas with limited expertise. The main applications of these could be (1) improved seizure detection methods; (2) refined semiology analysis for predicting seizure type and cerebral localization. In this paper, we detail the foundation technologies used in vision-based systems in the analysis of seizure videos, highlighting their success in semiology detection and analysis, focusing on work published in the last 7 years. We systematically present these methods and indicate how the adoption of deep learning for the analysis of video recordings of seizures could be approached. Additionally, we illustrate how existing technologies can be interconnected through an integrated system for video-based semiology analysis. Each module can be customized and improved by adapting more accurate and robust deep learning approaches as these evolve. Finally, we discuss challenges and research directions for future studies.

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.

Comparative Brain Morphology of Cleaning and Sponge-Dwelling Elacatinus Gobies.

INTRODUCTION: Comparative studies of brain anatomy between closely related species have been very useful in demonstrating selective changes in brain structure. Within-species comparisons can be particularly useful for identifying changes in brain structure caused by contrasting environmental selection pressures. Here, we aimed to understand whether differences within and between species in habitat use and foraging behaviour influence brain morphology, on both ecological and evolutionary time scales. METHODS: We used as a study model three species of the Elacatinus genus that differ in their habitat-foraging mode. The obligatory cleaning goby Elacatinus evelynae inhabits mainly corals and feeds mostly on ectoparasites removed from larger fish during cleaning interactions. In contrast, the obligatory sponge-dwelling goby Elacatinus chancei inhabits tubular sponges and feeds on microinvertebrates buried in the sponges' tissues. Finally, in the facultatively cleaning goby Elacatinus prochilos, individuals can adopt either phenotype, the cleaning or the sponge-dwelling habitat-foraging mode. By comparing the brains of the facultative goby phenotypes to the brains of the obligatory species we can test whether brain morphology is better predicted by phylogenetic relatedness or the habitat-foraging modes (cleaning × sponge dwelling). RESULTS: We found that E. prochilos brains from both types (cleaning and sponge dwelling) were highly similar to each other. Their brains were in general more similar to the brains of the most closely related species, E. evelynae (obligatory cleaning species), than to the brains of E. chancei (sponge-dwelling species). In contrast, we found significant brain structure differences between the cleaning species (E. evelynae and E. prochilos) and the sponge-dwelling species (E. chancei). These differences revealed independent changes in functionally correlated brain areas that might be ecologically adaptive. E. evelynae and E. prochilos had a relatively larger visual input processing brain axis and a relatively smaller lateral line input processing brain axis than E. chancei. CONCLUSION: The similar brain morphology of the two types of E. prochilos corroborates other studies showing that individuals of both types can be highly plastic in their social and foraging behaviours. Our results in the Elacatinus species suggest that morphological adaptations of the brain are likely to be found in specialists whereas species that are more flexible in their habitat may only show behavioural plasticity without showing anatomical differences.

Monarch butterflies memorize the spatial location of a food source.

Spatial memory helps animals to navigate familiar environments. In insects, spatial memory has extensively been studied in central place foragers such as ants and bees. However, if butterflies memorize a spatial location remains unclear. Here, we conducted behavioural experiments to test whether monarch butterflies (Danaus plexippus) can remember and retrieve the spatial location of a food source. We placed several visually identical feeders in a flight cage, with only one feeder providing sucrose solution. Across multiple days, individual butterflies predominantly visited the rewarding feeder. Next, we displaced a salient landmark close to the feeders to test which visual cue the butterflies used to relocate the rewarding feeder. While occasional landmark displacements were ignored by the butterflies and did not affect their decisions, systematic displacement of both the landmark and the rewarding feeder demonstrated that the butterflies associated the salient landmark with the feeder's position. Altogether, we show that butterflies consolidate and retrieve spatial memory in the context of foraging.

Comparative biology of spatial navigation in three arachnid orders (Amblypygi, Araneae, and Scorpiones).

From both comparative biology and translational research perspectives, there is escalating interest in understanding how animals navigate their environments. Considerable work is being directed towards understanding the sensory transduction and neural processing of environmental stimuli that guide animals to, for example, food and shelter. While much has been learned about the spatial orientation behavior, sensory cues, and neurophysiology of champion navigators such as bees and ants, many other, often overlooked animal species possess extraordinary sensory and spatial capabilities that can broaden our understanding of the behavioral and neural mechanisms of animal navigation. For example, arachnids are predators that often return to retreats after hunting excursions. Many of these arachnid central-place foragers are large and highly conducive to scientific investigation. In this review we highlight research on three orders within the Class Arachnida: Amblypygi (whip spiders), Araneae (spiders), and Scorpiones (scorpions). For each, we describe (I) their natural history and spatial navigation, (II) how they sense the world, (III) what information they use to navigate, and (IV) how they process information for navigation. We discuss similarities and differences among the groups and highlight potential avenues for future research.

The archerfish predictive C-start.

A very quick decision enables hunting archerfish to secure downed prey even when they are heavily outnumbered by competing other surface-feeding fish. Based exclusively on information that is taken briefly after the onset of prey motion, the fish select a rapid C-start that turns them right towards the later point of catch. Moreover, the C-start, and not later fin strokes, already lends the fish the speed needed to arrive at just the right time. The archerfish predictive C-starts are kinematically not distinguishable from escape C-starts made by the same individual and are among the fastest C-starts known in teleost fish. The start decisions allow the fish-for ballistically falling prey-to respond accurately to any combination of the initial variables of prey movement and for any position and orientation of the responding fish. The start decisions do not show a speed-accuracy tradeoff and their accuracy is buffered against substantial changes of environmental parameters. Here, I introduce key aspects of this high-speed decision that combines speed, complexity, and precision in an unusual way.

The Presidential Symposium at the International Congress of Neuroethology 2022 in Lisbon, Portugal.

In this special issue of articles from leading neuroethologists-all of whom gave outstanding presentations within the Presidential Symposium of the 2022 International Congress of Neuroethology held in Lisbon, Portugal-we learn about the role of cryptochrome molecules in the magnetic sense of animals, how honeybees construct their honeycombs, why fish eyes are built the way they are in species from different depths, how archerfish intercept their newly downed prey with a swift muscular curving of the body (known as a C-start) and how birds process optic flow information to control flight. Each contribution showcases how nervous systems have evolved to control behaviour, the raison d'être of neuroethology.

'Distributed' vision and the architecture of animal visual systems.

More than a century of research, of which JEB has published a substantial selection, has highlighted the rich diversity of animal eyes. From these studies have emerged numerous examples of visual systems that depart from our own familiar blueprint, a single pair of lateral cephalic eyes. It is now clear that such departures are common, widespread and highly diverse, reflecting a variety of different eye types, visual abilities and architectures. Many of these examples have been described as 'distributed' visual systems, but this includes several fundamentally different systems. Here, I re-examine this term, suggest a new framework within which to evaluate visual system distribution in both spatial and functional senses, and propose a roadmap for future work. The various architectures covered by this term reflect three broad strategies that offer different opportunities and require different approaches for study: the duplication of functionally identical eyes, the expression of multiple, functionally distinct eye types in parallel and the use of dispersed photoreceptors to mediate visual behaviour without eyes. Within this context, I explore some of the possible implications of visual system architecture for how visual information is collected and integrated, which has remained conceptually challenging in systems with a large degree of spatial and/or functional distribution. I highlight two areas that should be prioritised in future investigations: the whole-organism approach to behaviour and signal integration, and the evolution of visual system architecture across Metazoa. Recent advances have been made in both areas, through well-designed ethological experiments and the deployment of molecular tools.

Displacement experiments provide evidence for path integration in Drosophila.

Like many other animals, insects are capable of returning to previously visited locations using path integration, which is a memory of travelled direction and distance. Recent studies suggest that Drosophila can also use path integration to return to a food reward. However, the existing experimental evidence for path integration in Drosophila has a potential confound: pheromones deposited at the site of reward might enable flies to find previously rewarding locations even without memory. Here, we show that pheromones can indeed cause naïve flies to accumulate where previous flies had been rewarded in a navigation task. Therefore, we designed an experiment to determine if flies can use path integration memory despite potential pheromonal cues by displacing the flies shortly after an optogenetic reward. We found that rewarded flies returned to the location predicted by a memory-based model. Several analyses are consistent with path integration as the mechanism by which flies returned to the reward. We conclude that although pheromones are often important in fly navigation and must be carefully controlled for in future experiments, Drosophila may indeed be capable of performing path integration.

Polarization sensitivity and decentralized visual processing in an animal with a distributed visual system.

The marine mollusc Acanthopleura granulata (Mollusca; Polyplacophora) has a distributed visual array composed of hundreds of small image-forming eyes embedded within its eight dorsal shell plates. As in other animals with distributed visual systems, we still have a poor understanding of the visual capabilities of A. granulata and we have yet to learn where and how it processes visual information. Using behavioral trials involving isoluminant looming visual stimuli, we found that A. granulata demonstrates spatial vision with an angular resolution of 6 deg. We also found that A. granulata responds to looming stimuli defined by contrasting angles of linear polarization. To learn where and how A. granulata processes visual information, we traced optic nerves using fluorescent lipophilic dyes. We found that the optic nerves innervate the underlying lateral neuropil, a neural tissue layer that circumnavigates the body. Adjacent optic nerves innervate the lateral neuropil with highly overlapping arborizations, suggesting it is the site of an integrated visuotopic map. Using immunohistochemistry, we found that the lateral neuropil of A. granulata is subdivided into two separate layers. In comparison, we found that a chiton with eyespots (Chiton tuberculatus) and two eyeless chitons (Ischnochiton papillosus and Chaetopleura apiculata) have lateral neuropil that is a singular circular layer without subdivision, findings consistent with previous work on chiton neuroanatomy. Overall, our results suggest that A. granulata effectuates its visually mediated behaviors using a unique processing scheme: it extracts spatial and polarization information using a distributed visual system, and then integrates and processes that information using decentralized neural circuits.

pi_tailtrack: A compact, inexpensive and open-source behaviour-tracking system for head-restrained zebrafish.

Quantifying animal behaviour during microscopy is crucial to associate optically recorded neural activity with behavioural outputs and states. Here, I describe an imaging and tracking system for head-restrained larval zebrafish compatible with functional microscopy. This system is based on the Raspberry Pi computer, Pi NoIR camera and open-source software for the real-time tail segmentation and skeletonization of the zebrafish tail at over 100 Hz. This allows for precise and long-term analyses of swimming behaviour, which can be related to functional signals recorded in individual neurons. This system offers a simple but performant solution for quantifying the behaviour of head-restrained larval zebrafish, which can be built for 340€.

An 'instinct for learning': the learning flights and walks of bees, wasps and ants from the 1850s to now.

The learning flights and walks of bees, wasps and ants are precisely coordinated movements that enable insects to memorise the visual surroundings of their nest or other significant places such as foraging sites. These movements occur on the first few occasions that an insect leaves its nest. They are of special interest because their discovery in the middle of the 19th century provided perhaps the first evidence that insects can learn and are not solely governed by instinct. Here, we recount the history of research on learning flights from their discovery to the present day. The first studies were conducted by skilled naturalists and then, over the following 50 years, by neuroethologists examining the insects' learning behaviour in the context of experiments on insect navigation and its underlying neural mechanisms. The most important property of these movements is that insects repeatedly fixate their nest and look in other favoured directions, either in a preferred compass direction, such as North, or towards preferred objects close to the nest. Nest facing is accomplished through path integration. Memories of views along a favoured direction can later guide an insect's return to its nest. In some ant species, the favoured direction is adjusted to future foraging needs. These memories can then guide both the outward and homeward legs of a foraging trip. Current studies of central areas of the insect brain indicate what regions implement the behavioural manoeuvres underlying learning flights and the resulting visual memories.