This Special Issue of the Journal of Comparative Physiology A continues the journal’s tradition of recognizing pioneering neuroethologists by honoring Peter M. Narins. A former Associate Editor of the Journal and an influential colleague to researchers worldwide, Peter has profoundly shaped the field. The 21 papers collected here – authored by collaborators, friends, and former students – highlight how his signature integrative and evolutionary approach to the study of animal communication continues to inspire neuroethological research on anurans and other model species.
Many seasonal vertebrates rely on photoperiod to synchronise their seasonal physiology and behaviour with annual changes in the environment. In both mammals and birds, the pars tuberalis (PT) of the pituitary gland decodes photoperiodic information and regulates seasonal timing. It achieves this through thyroid-stimulating hormone (TSH) signalling to neighbouring hypothalamic glial cells known as tanycytes, which line the ventricular walls of the mediobasal hypothalamus (MBH) and express TSH receptors (TSHR). In turn, tanycytes govern the seasonal state of neural circuits controlling energy metabolism and reproduction. PT – MBH signalling interactions in addition to the TSH / TSHR axis have been suggested but conservation between mammals and birds has not been demonstrated. Here, we performed laser capture microdissection and transcriptomic analysis of PT and tanycyte-enriched MBH samples taken from one highly seasonal mammal, the Golden hamster, and from one highly seasonal bird, the Svalbard ptarmigan. Comparison of bidirectional G-protein coupled receptor (GPCR) – peptidergic ligand expression levels across summer and winter states reconfirmed the central role of TSH signalling as a conserved mechanism within the seasonal neuroendocrine pathway. In both species, ligand-receptor pairing analysis provides evidence for MBH signalling to the PT through somatostatin (Sst), chemerin (Rarres2) and neuropeptide Y (Npy) signalling pathways. Further analysis of cellular expression patterns and signalling function is warranted to determine whether these pathways play conserved roles in the expression of seasonal changes in metabolic or reproductive physiology.
A laboratory-based setup was developed that allowed us to train bumblebees to a rewarding object (local cue) in the context of a panorama and simultaneously to record extracellularly the neural activity of units interpreted as mushroom body extrinsic neurons (MBENs). This setting simulates conditions flower visiting bees face when foraging excluding the compass related conditions. The bumblebees navigated between the colony and the test/feeding arena on their own motivation, starting from a fully functional colony with a queen. They learned by sucrose reward a specific feeding place marked by the rewarding object local cue (blue pyramid cylinder) placed in a fixed spatial relation to the panorama (matching panorama). Spontaneous choice tests and extinction tests revealed enhanced search behavior for the learned matching condition. Single or multiple (up to three) simultaneously recorded neurons referred to here as units revealed learning-related differences either by increased, decreased or unchanged neural activity. We focused on tests in which the local cue was presented in the same area as the panorama (learned condition: matched) or in separate areas (mismatched condition). Neural activity differed in these two test conditions. This learning effect did not depend on the areas tested, indicating that the whole arena had been learned as an environment in which the local cue and the panorama were spatially related. No changes in neural activity were found for head direction toward the goal (local cue, panorama, matched or mismatched), distance to the goals or the gateway. No place-cell-like activity patterns were found. Significant neural effects were also seen in some units during multiple walks between local cue and panorama in mismatch tests.
From dense assemblages of vocalizing organisms in neotropical rainforests, to fast-flowing streams and waterfalls in the Old World, Peter Narins' work has been instrumental to our understanding of how animals, particularly frogs, communicate in noisy environments. With increasing levels of human-generated noise, there has been an explosion of studies on how vocal signals and signaling behaviors change in urban soundscapes. Surprisingly, we know little about changes in sensory-processing mechanisms of receivers. We asked whether vocal signals, hearing sensitivity, and the ability to extract signals from noise of Pacific treefrogs (Pseudacris regilla) vary in ways that facilitate communication among sites with different levels of urbanization and noise. We show that males from sites with high levels of urbanization and noise produce calls at higher rates and lower frequencies. Auditory brainstem responses obtained in the presence and absence of noise reveal that, at frequencies present in the vocalizations, subjects from urbanized and noisy sites are less sensitive and experience reduced masking. Our results suggest that lower auditory sensitivity may function as a gain-reduction mechanism that improves the signal-to-noise ratio in sites with high levels of ambient noise. We discuss our results considering Narins' contributions to anuran auditory neuroethology.
In rodent pups, ultrasonic vocalizations (USVs) are thought to function as contact signals in mother–infant communication, but it remains unclear whether early disruption of the social environment alters their communicative effectiveness. Using the Mongolian gerbils (Meriones unguiculatus), we examined whether early social deprivation (SD), consisting of 24-h individual isolation of a subset of pups from each litter from the dam and from physical interaction with littermates, alters pup USVs and maternal responses to them. Isolation-induced USVs were recorded longitudinally from 54 pups from 9 litters at postnatal days P7, P9, and P10, and acoustic features based on peak-frequency trajectories were quantified. In addition, a two-choice playback experiment was conducted in lactating dams using stimuli derived from P10 control and SD pups. SD affected both the quantity and acoustic structure of pup USVs. In particular, group differences became most evident at P10, when SD pups emitted fewer calls and showed reduced frequency-modulation related acoustic features. In the playback test, maternal approach-related responses were stronger to control-derived stimuli than to SD-derived stimuli. These findings suggest that early social deprivation alters pup vocal development and reduces the effectiveness of pup USVs in eliciting maternal responses, supporting the presence of experience-dependent plasticity in sender–receiver coupling in mammalian acoustic communication.
Visual patterns are widely deployed as non-chemical insect deterrents, yet the visual mechanism remains unresolved. We tested whether spatial aliasing, arising from a mismatch between stripe geometry and compound-eye sampling, disrupts landing control. Using trained honey bees (Apis mellifera) and three-dimensional trajectory tracking, we quantified search and landing/entry performance across stripe scale and orientation. Stripe scale produced a non-monotonic behavioural response: disruption was greatest at intermediate stripe widths ( 0.95–0.475 cm), where search times peaked and performance deteriorated. On a floor-mounted landing target, failures peaked at intermediate widths (up to 80
Left/right and front/back sound-localization thresholds, as well as the ability to use binaural time and intensity cues, are presented for one lagomorph (domestic rabbits) and five species of rodents (fox squirrel, black-tailed prairie dog, groundhog, eastern chipmunk, and spiny mouse). These localization abilities are compared to those of other mammals and all three are shown to vary widely. Many species do not localize as accurately as the available physical locus cues would seem to permit. Instead, localization acuity is negatively correlated with the width of the field of best vision. This coordination of hearing and vision allows auditory information on the location of sound sources to direct the reflexive orientation of vision and attention for further evaluation. It is possible that the coordination of hearing with vision drives the evolution of sound localization among mammals. Species differences in front/back discrimination are less well studied but also vary widely, and may be influenced by complex interactions between pinna size and complexity. Finally the use of interaural phase differences varies in unexpected ways raising questions about the anatomical and neural mechanisms that underlie binaural analysis in the nervous system.
Courtship in frogs can mediate the final approach between the sexes before amplexus and spawning. It can involve male and female calling, touching, and guidance to the spawning site. Courtship behaviors have been described for several species in nature but little experimentation has been done to uncover the biological mechanisms that control them. We characterized the close-range courtship (within 10 cm) interactions in the túngara frog, an emerging model organism, to provide a quantitative baseline in a neutral arena in support of future experiments. In this initial assessment, we isolated each pair to examine only the social stimulation that is intrinsic to the pair. Among 81 pairs, 80
Animals have evolved escape behaviors to survive. Freshwater planarians have many predators, including conspecifics in cannibalistic species such as Dugesia japonica. When agitated, planarians escape via a locomotory behavior called “scrunching”, whereby the planarian periodically elongates and contracts its whole body. Current understanding is that planarians move forward when they scrunch. However, when transversely cutting D. japonica, we observed that while head pieces scrunched forward, tail pieces scrunched backward instead. Previous work has shown that forward scrunching is a conserved planarian escape behavior in response to transection and adverse stimuli such as low pH, noxious heat, hydrogen peroxide, and allyl isothiocyanate. Testing these stimuli, we found that backward scrunching is more difficult to induce than forward scrunching in both intact planarians and pieces. Using electrostimulation, we show that behavior progresses with increasing voltage from turning to backward scrunching to flailing when stimulated anteriorly, demonstrating that backward scrunching is a response to moderately strong stimuli. Moreover, we show that tail pieces – originating from transection or asexual reproduction (fission) - exhibit backward scrunching when attacked by intact planarians. Backward scrunching and backward steps of tail pieces were also observed when worms were bitten into pieces by dragonfly or damselfly nymphs, natural predators of planarians. The survival of tail pieces after fission is necessary for the expansion of asexual planarian populations. Thus, we propose that backward scrunching serves as an effective escape behavior to protect planarian tails from being eaten.
The Surinam toad (Pipa pipa) is a fully aquatic, tongueless pipid frog that captures prey using rapid suction feeding coordinated by the forelimbs. The digit tips bear distinctive lobed structures whose function has been unknown. Here we characterize the morphology, mechanical sensitivity, peripheral innervation, central representation, and behavioral function of these digit tip lobes using scanning electron microscopy, von Frey threshold measurements, in vivo electrophysiology of the brachial nerve and optic tectum, and high-speed video analysis (1000 fps). SEM reveals a progressive quadrification yielding 128 terminal lobules per frog, bearing dome-shaped papillae at 142 ± 18/mm2—nearly fourfold the density on adjacent digit shaft skin. Distal lobule tips have the lowest mechanical thresholds on the forelimb (median 0.07 mN). Brachial nerve recordings reveal disproportionately represented, low-threshold, predominantly rapidly adapting mechanoreceptive afferents with small receptive fields confined to the lobules, some also responsive to water current stimulation. Tectal mapping shows the digit tips are somatotopically represented and disproportionately magnified, occupying 34
Analysis of flash-induced quantum bumps (QB) recorded in vivo from photoreceptors of the blow fly Protophormia terraenovae, which were light-adapted by stimuli of varying duration and intensity, revealed that a subset of trials contained a secondary QB-like transient occurring after the primary QB. By averaging traces with onset-aligned light-induced QBs, we discovered secondary signals with the following properties: (1) The relative magnitude of the secondary signal increased with both the intensity and the duration of the adapting stimulus. The secondary signal was absent in dark-adapted photoreceptors, but following bright 10 s adapting pulses its size approached 40
Echolocating big brown bats broadcast downward-sweeping, frequency-modulated (FM) biosonar sounds and process the returning echoes to track and capture flying insects. Neurons in the inferior colliculus are tuned to different frequencies along the FM sweep and form a representation of target azimuth largely on the basis of sensitivity to interaural differences in intensity, with canonical interaural time difference cues by themselves less reliable. Here, we reanalyze neurophysiological data on binaural sensitivity of inferior colliculus neurons consistent with a signal-processing model used in engineered sonar for generating directional beams. Model inputs are the times-of-occurrence of phasic-on responses to FM sweeps presented at a range of interaural intensities and azimuths. Tuning curves for interaural intensity were computed, and the slopes of these tuning curves plotted against neuronal best frequency and sound azimuth. The resulting aggregate plots suggest that the bat forms two distinct beams, one encompassing the entire FM sweep for a narrow zone of azimuths straight ahead and the other restricted to lower frequencies and offside to the left and the right. When interpreted with respect to psychophysical data, these analyses suggest that the forward beam allows for acute target perception, while the offside beams allow for perception of multiple objects that constitute clutter. The distribution of azimuths further suggests the formation of numerous detailed offside beams pointing in different directions to accommodate the width of the spatial arrangement of the clutter.
The pond snail Lymnaea stagnalis displays clear photoperiodism; it lays more eggs in long-day conditions than in short to medium-day conditions. The lateral lobes (LLs) are paired small budding structures of the cerebral ganglia and regulate egg laying as a coordinating center between reproduction and body growth, and LL ablation causes gigantism and attenuates egg laying. Our previous study demonstrated that the canopy cell (CC) in LL photoperiodically changes the excitability; it excites more in long-day conditions than in medium-day conditions. Here, we examined the function of CC in egg laying by the microsurgery. As a result, in long-day conditions, snails without CCs exhibited smaller albumen gland somatic index (ASI, proportion of the albumen gland/soft body) and smaller total number of egg masses laid than intact snails. In contrast, in medium-day conditions, there were no significant differences in ASI among intact, sham and CC ablation groups. Since the albumen gland produces galactogen-rich perivitelline fluid and supplies eggs with it, the CCs seem to promote egg mass production via acceleration of the perivitelline fluid production in long-day conditions. It is noteworthy that CC ablation had no effects on gonadal somatic index (GSI, proportion of the ovotestis/soft body). Besides, CC ablation caused slight increase in shell size and body weight. These imply that CCs are at least partially responsible for gigantism and decrement of egg laying caused by LL ablation, and we revealed another regulator in photoperiod-dependent egg laying in L. stagnalis. Our findings contribute to understanding neuroendocrine mechanisms underlying molluscan photoperiodism.
Acoustic distance estimation in vocal species is fundamental for effective decision-making for territory defense, mate attraction, and eavesdropping predators and parasites. The most straightforward distance cue is sound pressure level. However, variation in sound pressure level within individuals is not well documented, even less the call-by-call variation that may occur within individuals, even though modulation of call amplitude will promote responses to fluctuating ecological contexts and challenges. In this study, I report on the variable and unpredictable pattern of sound pressure levels in the advertisement calls of individual running frogs, Kassina fusca. The sound pressure levels of all advertisement calls within a single calling bout were recorded for nine males. Median peak SPL between males varied between 89.5 and 98.4 dB and showed highly significant differences between males. Furthermore, the maximum change in SPL between successive calls of a male ranged between 1.7 and 12.7 dB. Run charts of each male indicated random patterns of variation in SPL’s during the recorded call bout. The results of this study are best explained as a mechanism to interfere with accurate distance estimation, either by competitors, parasites, or predators.
Bats navigating clutter must steer around obstacles to avoid collision, while simultaneously planning future flight trajectories. In this study, we investigated active sensing strategies of two bat species negotiating turns under matched geometric constraints. We compare the Egyptian fruit bat (Rousettus aegyptiacus), a lingual echolocator that can actively direct its sonar beam axis using tongue driven mechanisms, and the short-tailed fruit bat (Carollia perspicillata), a laryngeal nasal echolocator whose head aim and nose leaf shape emission directionality. Bats flew through a felt lined, ‘L’ shaped corridor designed to elicit turns. A 32-channel ultrasonic array and 3D video tracking system captured their sonar emissions and flight trajectories. In both species, bats reduced flight speeds and increased angular deviation between sonar beam aim (acoustic gaze) and flight direction before the apex of high angle turns. A directional prediction analysis showed that sonar gaze reliably anticipated the direction of the subsequent heading change in both species (77
The brain regions supporting spatial navigation are well studied in mammals, but their function in the spatial behavior of other vertebrates is poorly understood, especially in field conditions. Here, we measured the behavior and neural correlates of the initial stages of navigation in a territorial rainforest frog, Allobates femoralis, in its natural environment. Frogs were released in familiar, unfamiliar, or home areas. Only frogs released in a familiar area, but outside their home territory, showed significant orientation towards home and spent more time on elevated structures, presumably orienting in space. In contrast, frogs released back in their home territory tended to move little, whereas those released in an unfamiliar area tended to move more, possibly exploring unfamiliar sites to find familiar landmarks. Contrary to our prediction, the amphibian homolog of the hippocampus (medial pallium) did not show a selective response to the navigational task. When accounting for behavioral differences, most measured pallial and subpallial regions showed increased neural activity during frog orientation home from a familiar environment. Interestingly, despite the behavioral differences, there were few differences in brain activity between the frogs released directly back home and those released in an unfamiliar area. Overall, we find that wild poison frogs respond selectively to environmental familiarity and that most measured brain regions have more translationally-active neurons when challenged to navigate a familiar setting. Our findings support the hypothesis that, in amphibians, brain regions homologous to mammalian centers of spatial processing exhibit more task-general responses.
Amblypygi (whip spiders) are an order of arthropods (Subphylum: Chelicerata, Class: Arachnida) that navigate primarily by their keen olfactory abilities. Experiments in the laboratory reveal that the species Phrynus marginemaculatus forms both short and long-term memories for odors associated with access to a shelter. While bioamine function and location in the whip spider nervous system remain completely unexplored, comparative anatomy indicates that their olfactory memory may involve serotonin and dopamine signaling in brain regions involved in processing olfactory input. Preliminary immunohistochemistry detected serotonin and tyrosine hydroxylase immunoreactivity in mushroom body-associated calycal regions and antenniform primary olfactory glomeruli, supporting future work on monoaminergic modulation of olfactory circuits. Therefore, if serotonin or dopamine signaling involved in olfactory processing is pharmacologically disrupted, their performance in an associative olfactory learning task should be significantly impaired. Subjects were trained on an olfactory memory paradigm, subsequently injected with physiological saline, the serotonin receptor antagonist methiothepin mesylate (MET), or the dopamine receptor antagonist SCH-23390 (SCH), and tested for memory retention 24 h afterwards. Controls injected with saline demonstrated robust associative memory (serotonin antagonism control: n = 10, p = 0.006 against chance performance on the task, dopamine antagonism control: n = 10, p = 0.039), while treated groups displayed no such memory (MET: n = 10, p = 0.375, SCH: n = 10, p = 0.892). There was also a significant difference in performance between the treated and control groups on test day (serotonin antagonism groups: p = 0.048, dopamine antagonism groups: p = 0.016). Additionally, there were no significant differences in locomotor activity between treatment and control groups on test day (p > 0.05). Together, these results are consistent with serotonergic and dopaminergic signaling contributing to olfactory memory consolidation without grossly impairing locomotion in Phrynus marginemaculatus.
Of the three otolithic organs found in frogs, the sacculus is known to possess acute sensitivity to seismic vibrations. Simple models of otolith function suggest that increasing size of an otolith should improve vibratory sensitivity. In the first part of this paper, we provide a short review of the existing literature pertaining to the vibratory sensitivity of the otolithic organs in frogs. Given parallels in other vertebrate groups, we hypothesized that fossorial frogs would have larger saccular otoconial masses (‘otoliths’) than non-burrowing species, used for the detection of ground vibrations. In the second part of this paper, we tested this hypothesis by measuring otolith volumes in 15 species of frogs, based on CT reconstructions. Larger species tended to have larger otoliths. The fossorial frog Hemisus guineensis had the largest otoliths relative to skull size of all species examined, followed by a non-fossorial species, Ptychadena delphina. The otoliths of two other fossorial specialists were not notably enlarged, however, and volumes were relatively small in some semi-fossorial species. Pronounced sexual dimorphism was noted in the aquatic frog Xenopus laevis, in which males have larger saccular otoliths than females in absolute terms, despite their smaller body size. Otoconial dissolution represents a problem for studies which involve the examination of preserved specimens, but with this caveat in mind, we conclude that factors other than fossoriality might drive expansion of the saccular otoliths in frogs.
Studies in ranid frogs have shown clear patterns of responses to sound direction in midbrain auditory neurons, in consonance with the ability of males and females to locate sound sources. To explore the diversity and extent of such neuronal mechanisms, we recorded directional single-unit responses of torus semicircularis auditory neurons in the leptodactylid frogs Pleurodema thaul and Eupsophus calcaratus which produce amplitude modulated and tonal advertisement calls, respectively. In both species the largest proportion of neurons respond preferentially to contralateral sound source locations. Directionality proportions were calculated from differences in spike counts produced by individual neurons to stimuli broadcast from different azimuth angles. E. calcaratus, but not P. thaul, gives higher directional responses to stimuli built with noise carrier relative to stimuli built with tone carrier. In addition, E. calcaratus gives higher directional responses to tonal and noise stimuli relative to P. thaul, however no difference in directionality occur in response to stimuli designed after the conspecific advertisement calls. The larger directionality of responses of E. calcaratus to noisy relative to tonal stimuli aligns with a general ability of vertebrates to localize better sounds containing broad spectra. The larger directionality of neuronal responses of E. calcaratus relative to P. thaul could relate to the sharper contrast between the noisy stimuli and the tonal structure of the advertisement call of this frog. These results expand the knowledge on neuronal sound localization ability of frogs, as studies on this issue had so far been restricted to a few ranid species.
Acoustic communication in anurans is energetically costly and constrained by environmental factors, especially in open savanna ecosystems where extreme temperature fluctuations, desiccation risks, and wind-induced noise pose significant challenges to signal propagation and caller physiology. We analyzed the acoustic ecology of the widespread bubbling Kassina (Kassina senegalensis) in Mozambique, and compared it with that of other locations. We examined the influence of temperature, photoperiod and moonlight on calling phenology. Calling phenology was strongly seasonal driven, while daily patterns showed a bimodal strategy with peaks at dawn and dusk. This crepuscular activity suggests a behavioral adaptation to optimize signal transmission during stable atmospheric conditions and/or reducing desiccation. We identified a thermal window for vocalization ( 23–27 °C), with activity sharply declining above 30 °C, suggesting a physiological upper limit. Moonlight also had an effect on calling activity. These findings highlight the behavioral and physiological plasticity of K. senegalensis in navigating savanna constraints, offering insights into ectotherm neuroethological adaptations amid climate change.
