Getting a glimpse into the sensory worlds of animals: the Editors' and Readers' Choice Awards 2024.

The Editors' and Readers' Choice Awards were established in 2022 to celebrate some of the outstanding articles published every year in the Journal of Comparative Physiology A. The recipients of the 2024 Editors' Choice Awards were selected based on votes cast by the Editorial Board on articles published in 2023. In the category Original Paper, this distinction goes to 'Views from 'crabworld': the spatial distribution of light in a tropical mudflat' by Jochen Zeil (J Comp Physiol A 209:859-876, 2023); and in the category Review Article to 'Olfactory navigation in arthropods' by Theresa J. Steele and colleagues (J Comp Physiol A 209:467-488, 2023). The winners of the 2024 Readers' Choice Awards were determined by the number of online accesses of articles published in 2022. In the category Original Paper, the winner is 'Broadband 75-85 MHz radiofrequency fields disrupt magnetic compass orientation in night­migratory songbirds consistent with a flavin­based radical pair magnetoreceptor' by Bo Leberecht and colleagues (J Comp Physiol A 208:97-106, 2022). In the category Review Article, the winner is 'Magnetic maps in animal navigation' by Kenneth J. Lohmann and colleagues (J Comp Physiol A 208:41-67, 2022), which already won the Editors' Choice Award in 2023.

Anatomical organization of the cerebrum of the praying mantis Hierodula membranacea.

Many predatory animals, such as the praying mantis, use vision for prey detection and capture. Mantises are known in particular for their capability to estimate distances to prey by stereoscopic vision. While the initial visual processing centers have been extensively documented, we lack knowledge on the architecture of central brain regions, pivotal for sensory motor transformation and higher brain functions. To close this gap, we provide a three-dimensional (3D) reconstruction of the central brain of the Asian mantis, Hierodula membranacea. The atlas facilitates in-depth analysis of neuron ramification regions and aides in elucidating potential neuronal pathways. We integrated seven 3D-reconstructed visual interneurons into the atlas. In total, 42 distinct neuropils of the cerebrum were reconstructed based on synapsin-immunolabeled whole-mount brains. Backfills from the antenna and maxillary palps, as well as immunolabeling of γ-aminobutyric acid (GABA) and tyrosine hydroxylase (TH), further substantiate the identification and boundaries of brain areas. The composition and internal organization of the neuropils were compared to the anatomical organization of the brain of the fruit fly (Drosophila melanogaster) and the two available brain atlases of Polyneoptera-the desert locust (Schistocerca gregaria) and the Madeira cockroach (Rhyparobia maderae). This study paves the way for detailed analyses of neuronal circuitry and promotes cross-species brain comparisons. We discuss differences in brain organization between holometabolous and polyneopteran insects. Identification of ramification sites of the visual neurons integrated into the atlas supports previous claims about homologous structures in the optic lobes of flies and mantises.

One hundred years of excellence: the top one hundred authors of the Journal of Comparative Physiology A.

The Journal of Comparative Physiology A is the premier peer-reviewed scientific journal in comparative physiology, in particular sensory physiology, neurophysiology, and neuroethology. Founded in 1924 by Karl von Frisch and Alfred Kühn, it celebrates its 100th anniversary in 2024. During these 100 years, many of the landmark achievements in these disciplines were published in this journal. To commemorate these accomplishments, we have compiled a list of the Top 100 Authors over these 100 years, representing approximately 1% of all its authors. To select these individuals, three performance criteria were applied: number of publications, total number of citations attracted by these articles, and mean citation rate of the papers published by each author. The resulting list of the Top 100 Authors provides a fascinating insight into the history of the disciplines covered by the Journal of Comparative Physiology A and into the academic careers of many of their leading representatives.

Neuroarchitecture of the central complex in the Madeira cockroach Rhyparobia maderae: Pontine and columnar neuronal cell types.

Insects have evolved remarkable abilities to navigate over short distances and during long-range seasonal migrations. The central complex (CX) is a navigation center in the insect brain that controls spatial orientation and directed locomotion. It is composed of the protocerebral bridge (PB), the upper (CBU) and lower (CBL) division of the central body, and a pair of noduli. While most of its functional organization and involvement in head-direction coding has been obtained from work on flies, bees, and locusts that largely rely on vision for navigation, little contribution has been provided by work on nocturnal species. To close this gap, we have investigated the columnar organization of the CX in the cockroach Rhyparobia maderae. Rhyparobia maderae is a highly agile nocturnal insect that relies largely but not exclusively on antennal information for navigation. A particular feature of the cockroach CX is an organization of the CBU and CBL into interleaved series of eight and nine columns. Single-cell tracer injections combined with imaging and 3D analysis revealed five systems of pontine neurons connecting columns along the vertical and horizontal axis and 18 systems of columnar neurons with topographically organized projection patterns. Among these are six types of neurons with no correspondence in other species. Many neurons send processes into the anterior lip, a brain area highly reduced in bees and unknown in flies. While sharing many features with the CX in other species, the cockroach CX shows some unique attributes that may be related to the ecological niche of this insect.

Organization of descending neurons in the brain of the desert locust.

In most animals, multiple external and internal signals are integrated by the brain, transformed and, finally, transmitted as commands to motor centers. In insects, the central complex is a motor control center in the brain, involved in decision-making and goal-directed navigation. In desert locusts, it encodes celestial cues in a compass-like fashion indicating a role in sky-compass navigation. While several descending brain neurons (DBNs) including two neurons transmitting sky compass signals have been identified in the locust, a complete analysis of DBNs and their relationship to the central complex is still lacking. As a basis for further studies, we used Neurobiotin tracer injections into a neck connective to map the organization of DBNs in the brain. Cell counts revealed a maximum of 324 bilateral pairs of DBNs with somata distributed in 14 ipsilateral and nine contralateral groups. These neurons invaded most brain neuropils, especially the posterior slope, posterior and ventro-lateral protocerebrum, the antennal mechanosensory and motor center, but less densely the lateral accessory lobes that are targeted by central-complex outputs. No arborizations were found in the central complex and only few processes in the mushroom body, antennal lobe, lobula, medulla, and superior protocerebrum. Double label experiments provide evidence for the presence of GABA, dopamine, tyramine, but not serotonin, in small sets of DBNs. The data show that some DBNs may be targeted directly by central-complex outputs, but many others are likely only indirectly influenced by central-complex networks, in addition to input from multiple other brain areas.

Comparative morphology of serotonin-immunoreactive neurons innervating the central complex in the brain of dicondylian insects.

Serotonin (5-hydroxytryptamine) acts as a widespread neuromodulator in the nervous system of vertebrates and invertebrates. In insects, it promotes feeding, enhances olfactory sensitivity, modulates aggressive behavior, and, in the central complex of Drosophila, serves a role in sleep homeostasis. In addition to a role in sleep-wake regulation, the central complex has a prominent role in spatial orientation, goal-directed locomotion, and navigation vector memory. To further understand the role of serotonergic signaling in this brain area, we analyzed the distribution and identity of serotonin-immunoreactive neurons across a wide range of insect species. While one bilateral pair of tangential neurons innervating the central body was present in all species studied, a second type was labeled in all neopterans but not in dragonflies and firebrats. Both cell types show conserved major fiber trajectories but taxon-specific differences in dendritic targets outside the central body and axonal terminals in the central body, noduli, and lateral accessory lobes. In addition, numerous tangential neurons of the protocerebral bridge were labeled in all studied polyneopteran species except for Phasmatodea, but not in Holometabola. Lepidoptera and Diptera showed additional labeling of two bilateral pairs of neurons of a third type. The presence of serotonin in systems of columnar neurons apparently evolved independently in dragonflies and desert locusts. The data suggest distinct evolutionary changes in the composition of serotonin-immunolabeled neurons of the central complex and provides a promising basis for a phylogenetic study in a wider range of arthropod species.

Integration of optic flow into the sky compass network in the brain of the desert locust.

Flexible orientation through any environment requires a sense of current relative heading that is updated based on self-motion. Global external cues originating from the sky or the earth's magnetic field and local cues provide a reference frame for the sense of direction. Locally, optic flow may inform about turning maneuvers, travel speed and covered distance. The central complex in the insect brain is associated with orientation behavior and largely acts as a navigation center. Visual information from global celestial cues and local landmarks are integrated in the central complex to form an internal representation of current heading. However, it is less clear how optic flow is integrated into the central-complex network. We recorded intracellularly from neurons in the locust central complex while presenting lateral grating patterns that simulated translational and rotational motion to identify these sites of integration. Certain types of central-complex neurons were sensitive to optic-flow stimulation independent of the type and direction of simulated motion. Columnar neurons innervating the noduli, paired central-complex substructures, were tuned to the direction of simulated horizontal turns. Modeling the connectivity of these neurons with a system of proposed compass neurons can account for rotation-direction specific shifts in the activity profile in the central complex corresponding to turn direction. Our model is similar but not identical to the mechanisms proposed for angular velocity integration in the navigation compass of the fly Drosophila.

Unraveling the neural basis of spatial orientation in arthropods.

The neural basis underlying spatial orientation in arthropods, in particular insects, has received considerable interest in recent years. This special issue of the Journal of Comparative Physiology A seeks to take account of these developments by presenting a collection of eight review articles and eight original research articles highlighting hotspots of research on spatial orientation in arthropods ranging from flies to spiders and the underlying neural circuits. The contributions impressively illustrate the wide range of tools available to arthropods extending from specific sensory channels to highly sophisticated neural computations for mastering complex navigational challenges.

Neurons sensitive to non-celestial polarized light in the brain of the desert locust.

Owing to alignment of rhodopsin in microvillar photoreceptors, insects are sensitive to the oscillation plane of polarized light. This property is used by many species to navigate with respect to the polarization pattern of light from the blue sky. In addition, the polarization angle of light reflected from shiny surfaces such as bodies of water, animal skin, leaves, or other objects can enhance contrast and visibility. Whereas photoreceptors and central mechanisms involved in celestial polarization vision have been investigated in great detail, little is known about peripheral and central mechanisms of sensing the polarization angle of light reflected from objects and surfaces. Desert locusts, like other insects, use a polarization-dependent sky compass for navigation but are also sensitive to polarization angles from horizontal directions. In order to further analyze the processing of polarized light reflected from objects or water surfaces, we tested the sensitivity of brain interneurons to the angle of polarized blue light presented from ventral direction in locusts that had their dorsal eye regions painted black. Neurons encountered interconnect the optic lobes, invade the central body, or send descending axons to the ventral nerve cord but are not part of the polarization vision pathway involved in sky-compass coding.

Contact chemoreception, magnetic maps, thermoregulation by a superorganism, and, thanks to Einstein, an all-time record: the Editors' and Readers' Choice Awards 2023.

During the 99 years of its history, the Journal of Comparative Physiology A has published many of the most influential papers in comparative physiology and related disciplines. To celebrate this achievement of the journal's authors, annual Editors' Choice Awards and Readers' Choice Awards are presented. The winners of the 2023 Editors' Choice Awards are 'Contact chemoreception in multi­modal sensing of prey by Octopus' by Buresch et al. (J Comp Physiol A 208:435-442, 2022) in the Original Paper category; and 'Magnetic maps in animal navigation' by Lohmann et al. (J Comp Physiol A 208:41-67, 2022) in the Review/Review-History Article category. The winners of the 2023 Readers' Choice Awards are 'Coping with the cold and fighting the heat: thermal homeostasis of a superorganism, the honeybee colony' by Stabentheiner et al. (J Comp Physiol A 207:337-351; 2021) in the Original Paper category; and 'Einstein, von Frisch and the honeybee: a historical letter comes to light' by Dyer et al. (J Comp Physiol A 207:449-456, 2021) in the Review/Review-History category.

The sky compass network in the brain of the desert locust.

Many arthropods and vertebrates use celestial signals such as the position of the sun during the day or stars at night as compass cues for spatial orientation. The neural network underlying sky compass coding in the brain has been studied in great detail in the desert locust Schistocerca gregaria. These insects perform long-range migrations in Northern Africa and the Middle East following seasonal changes in rainfall. Highly specialized photoreceptors in a dorsal rim area of their compound eyes are sensitive to the polarization of the sky, generated by scattered sunlight. These signals are combined with direct information on the sun position in the optic lobe and anterior optic tubercle and converge from both eyes in a midline crossing brain structure, the central complex. Here, head direction coding is achieved by a compass-like arrangement of columns signaling solar azimuth through a 360° range of space by combining direct brightness cues from the sun with polarization cues matching the polarization pattern of the sky. Other directional cues derived from wind direction and internal self-rotation input are likely integrated. Signals are transmitted as coherent steering commands to descending neurons for directional control of locomotion and flight.

3D-atlas of the brain of the cockroach Rhyparobia maderae.

The Madeira cockroach Rhyparobia maderae is a nocturnal insect and a prominent model organism for the study of circadian rhythms. Its master circadian clock, controlling circadian locomotor activity and sleep-wake cycles, is located in the accessory medulla of the optic lobe. For a better understanding of brain regions controlled by the circadian clock and brain organization of this insect in general, we created a three-dimensional (3D) reconstruction of all neuropils of the cerebral ganglia based on anti-synapsin and anti-γ-aminobutyric acid immunolabeling of whole mount brains. Forty-nine major neuropils were identified and three-dimensionally reconstructed. Single-cell dye fills complement the data and provide evidence for distinct subdivisions of certain brain areas. Most neuropils defined in the fruit fly Drosophila melanogaster could be distinguished in the cockroach as well. However, some neuropils identified in the fruit fly do not exist as distinct entities in the cockroach while others are lacking in the fruit fly. In addition to neuropils, major fiber systems, tracts, and commissures were reconstructed and served as important landmarks separating brain areas. Being a nocturnal insect, R. maderae is an important new species to the growing collection of 3D insect brain atlases and only the second hemimetabolous insect, for which a detailed 3D brain atlas is available. This atlas will be highly valuable for an evolutionary comparison of insect brain organization and will greatly facilitate addressing brain areas that are supervised by the circadian clock.

Myoinhibitory peptides in the central complex of the locust Schistocerca gregaria and colocalization with locustatachykinin-related peptides.

The central complex in the brain of insects provides a neural network for sensorimotor processing that is essential for spatial navigation and locomotion and plays a role in sleep control. Studies on the neurochemical architecture of the central complex have been performed especially in the fruit fly Drosophila melangoaster and the desert locust, Schistocerca gregaria. In several insect species, myoinhibitory peptides (MIPs) are involved in circadian control and sleep-wake regulation. To identify neurons that might underlie these functions, we investigated the distribution of MIPs in the central complex of the locust. In silico transcript analysis suggests the presence of eight different MIPs in the desert locust. Through immunolabeling, we identified five systems of central-complex neurons that express MIP-like peptides. Two systems constitute columnar neurons of the protocerebral bridge and the lower division of the central body, while the other three systems are columnar neurons (two systems) and tangential neurons (one system) of the upper division of the central body. The innervation pattern and cell count of two systems of columnar neurons revealed the existence of 18 instead of 16 columns of the protocerebral bridge. Immunostaining of preparations containing intracellularly stained single cells allowed us to further specify subtypes of labeled columnar neurons. Double-label experiments showed that three systems of MIP-immunostained columnar neurons are also locustatachykinin-immunoreactive. No colocalization was found with serotonin immunostaining. The data provide novel insights into the architecture of the locust central complex and suggest that MIPs play a prominent role within the central-complex network.

It's all about seeing and hearing: the Editors' and Readers' Choice Awards 2022.

This year marks the inauguration of the annual Editors' Choice Award and the Readers' Choice Award, each presented for outstanding original papers and review articles published in the Journal of Comparative Physiology A. The winners of the 2022 Editors' Choice Award were determined by vote of the Editorial Board for the most highly recommended papers published in Volume 207 in 2021. They are 'Visual discrimination and resolution in freshwater stingrays (Potamotrygon motoro)' by Daniel et al. (J Comp Physiol A 207, 43-58, 2021) in the Original Paper category; and 'Neurophysiology goes wild: from exploring sensory coding in sound proof rooms to natural environments' by Römer (J Comp Physiol A 207, 303-319, 2021) in the Review Article category. The 2022 Readers' Choice Award was based on access number of articles published in Volume 206 in 2020, to ensure at least 12-month online presence. It is given to Nicholas et al. for their original paper titled 'Visual motion sensitivity in descending neurons in the hoverfly' (J Comp Physiol A 206, 149-163, 2020); and to Schnaitmann et al. for their review article entitled 'Color vision in insects: insights from Drosophila' (J Comp Physiol A 206, 183-198, 2020).

Performance of polarization-sensitive neurons of the locust central complex at different degrees of polarization.

The polarization pattern of the sky is exploited by many insects for spatial orientation and navigation. It derives from Rayleigh scattering in the atmosphere and depends directly on the position of the sun. In the insect brain, the central complex (CX) houses neurons tuned to the angle of polarization (AoP), that together constitute an internal compass for celestial navigation. Polarized light is not only characterized by the AoP, but also by the degree of polarization (DoP), which can be highly variable, depending on sky conditions. Under a clear sky, the DoP of polarized sky light may reach up to 0.75 but is usually much lower especially when light is scattered by clouds or haze. To investigate how the polarization-processing network of the CX copes with low DoPs, we recorded intracellularly from neurons of the locust CX at different stages of processing, while stimulating with light of different DoPs. Significant responses to polarized light occurred down to DoPs of 0.05 indicating reliable coding of the AoP even at unfavorable sky conditions. Moreover, we found that the activity of neurons at the CX input stage may be strongly influenced by nearly unpolarized light, while the activity of downstream neurons appears less affected.

Receptive field structures for two celestial compass cues at the input stage of the central complex in the locust brain.

Successful navigation depends on an animal's ability to perceive its spatial orientation relative to visual surroundings. Heading direction in insects is represented in the central complex (CX), a navigation center in the brain, to generate steering commands. In insects that navigate relative to sky compass signals, CX neurons are tuned to celestial cues indicating the location of the sun. The desert locust CX contains a compass-like representation of two related celestial cues: the direction of unpolarized direct sunlight and the pattern of polarized light, which depends on the sun position. Whether congruent tuning to these two compass cues emerges within the CX network or is inherited from CX input neurons is unclear. To address this question, we intracellularly recorded from GABA-immunoreactive TL neurons, which are input elements to the locust CX (corresponding to R neurons in Drosophila), while applying visual stimuli simulating unpolarized sunlight and polarized light across the hemisphere above the animal. We show that TL neurons have large receptive fields for both types of stimuli. However, faithful integration of polarization angles across the dorsal hemisphere, or matched-filter ability to encode particular sun positions, was found in only two out of 22 recordings. Those two neurons also showed a good match in sun position coding through polarized and unpolarized light signaling, whereas 20 neurons showed substantial mismatch in signaling of the two compass cues. The data, therefore, suggest that considerable refinement of azimuth coding based on sky compass signals occurs at the synapses from TL neurons to postsynaptic CX compass neurons.

The velvet worm brain unveils homologies and evolutionary novelties across panarthropods.

BACKGROUND: The evolution of the brain and its major neuropils in Panarthropoda (comprising Arthropoda, Tardigrada and Onychophora) remains enigmatic. As one of the closest relatives of arthropods, onychophorans are regarded as indispensable for a broad understanding of the evolution of panarthropod organ systems, including the brain, whose anatomical and functional organisation is often used to gain insights into evolutionary relations. However, while numerous recent studies have clarified the organisation of many arthropod nervous systems, a detailed investigation of the onychophoran brain with current state-of-the-art approaches is lacking, and further inconsistencies in nomenclature and interpretation hamper its understanding. To clarify the origins and homology of cerebral structures across panarthropods, we analysed the brain architecture in the onychophoran Euperipatoides rowelli by combining X-ray micro-computed tomography, histology, immunohistochemistry, confocal microscopy, and three-dimensional reconstruction. RESULTS: Here, we use this detailed information to generate a consistent glossary for neuroanatomical studies of Onychophora. In addition, we report novel cerebral structures, provide novel details on previously known brain areas, and characterise further structures and neuropils in order to improve the reproducibility of neuroanatomical observations. Our findings support homology of mushroom bodies and central bodies in onychophorans and arthropods. Their antennal nerve cords and olfactory lobes most likely evolved independently. In contrast to previous reports, we found no evidence for second-order visual neuropils, or a frontal ganglion in the velvet worm brain. CONCLUSION: We imaged the velvet worm nervous system at an unprecedented level of detail and compiled a comprehensive glossary of known and previously uncharacterised neuroanatomical structures to provide an in-depth characterisation of the onychophoran brain architecture. We expect that our data will improve the reproducibility and comparability of future neuroanatomical studies.

Distribution and daily oscillation of GABA in the circadian system of the cockroach Rhyparobia maderae.

Gamma-aminobutyric acid (GABA) is the prevalent inhibitory neurotransmitter in nervous systems promoting sleep in both mammals and insects. In the Madeira cockroach, sleep-wake cycles are controlled by a circadian clock network in the brain's optic lobes, centered in the accessory medulla (AME) with its innervating pigment-dispersing factor (PDF) expressing clock neurons at the anterior-ventral rim of the medulla. GABA is present in cell clusters that innervate different circuits of the cockroach's AME clock, without colocalizing in PDF clock neurons. Physiological, immunohistochemical, and behavioral assays provided evidence for a role of GABA in light entrainment, possibly via the distal tract that connects the AME's glomeruli to the medulla. Furthermore, GABA was implemented in clock outputs to multiple effector systems in optic lobe and midbrain. Here, GABAergic brain circuits were analyzed further, focusing on the circadian system in search for sleep/wake controlling brain circuits. All GABA-immunoreactive neurons of the cockroach brain were also stained with an antiserum against the GABA-synthesizing enzyme glutamic acid decarboxylase. We found strong overlap of the distribution of GABA-immunoreactive networks with PDF clock networks in optic lobes and midbrain. Neurons in five of the six soma groups that innervate the clock exhibited GABA immunoreactivity. The intensity of GABA immunoreactivity in the distal tract showed daily fluctuations with maximum staining intensity in the middle of the day and weakest staining at the end of the day. Quantification via enzyme-linked immunosorbent assay and quantitative liquid chromatography coupled to electrospray ionization tandem mass spectrometry, likewise, showed higher GABA levels in the optic lobe during the inactivity phase of the cockroach during the day and lower levels during its activity phase at dusk. Our data further support the hypothesis that light- and PDF-dependently the circadian clock network of the cockroach controls GABA levels and thereby promotes sleep during the day.

A unified platform to manage, share, and archive morphological and functional data in insect neuroscience.

Insect neuroscience generates vast amounts of highly diverse data, of which only a small fraction are findable, accessible and reusable. To promote an open data culture, we have therefore developed the InsectBrainDatabase (IBdb), a free online platform for insect neuroanatomical and functional data. The IBdb facilitates biological insight by enabling effective cross-species comparisons, by linking neural structure with function, and by serving as general information hub for insect neuroscience. The IBdb allows users to not only effectively locate and visualize data, but to make them widely available for easy, automated reuse via an application programming interface. A unique private mode of the database expands the IBdb functionality beyond public data deposition, additionally providing the means for managing, visualizing, and sharing of unpublished data. This dual function creates an incentive for data contribution early in data management workflows and eliminates the additional effort normally associated with publicly depositing research data.

Insect neuroscience, like any field in the natural sciences, generates vast amounts of data. Currently, only a fraction are publicly available, and even less are reusable. This is because insect neuroscience data come in many formats and from many species. Some experiments focus on what insect brains look like (morphology), while others focus on how insect brains work (function). Some data come in the form of high-speed video, while other data contain voltage traces from individual neurons. Sharing is not as simple as uploading the raw files to the internet. To get a clear picture of how insect brains work, researchers need a way to cross-reference and connect different experiments. But, as it stands, there is no dedicated place for insect neuroscientists to share and explore such a diverse body of work. The community needs an open data repository that can link different types of data across many species, and can evolve as more data become available. Above all, this repository needs to be easy for researchers to use. To meet these specifications, Heinze et al. developed the Insect Brain Database. The database organizes data into three categories: species, brain structures, and neuron types. Within these categories, each entry has its own profile page. These pages bring different experiments together under one heading, allowing researchers to combine and compare data of different types. As researchers add more experiments, the profile pages will grow and evolve. To make the data easy to navigate, Heinze et al. developed a visual search tool. A combination of 2D and 3D images allow users to explore the data by anatomical location, without the need for expert knowledge. Researchers also have the option to upload their work in private mode, allowing them to securely share unpublished data. The Insect Brain Database brings data together in a way that is accessible not only to researchers, but also to students, and non-scientists. It will help researchers to find related work, to reuse existing data, and to build an open data culture. This has the potential to drive new discoveries combining research across the whole of the insect neuroscience field.