Neuroethological Research Research Articles

Synaptic ring attractor: A unified framework for attractor dynamics and multiple cues integration

Effective cue integration is essential for an animal's survival. The ring attractor network has emerged as a powerful framework for understanding how animals seamlessly integrate various cues. This network not only elucidates neural dynamics within the brain, especially in spatial encoding systems like the heading direction (HD) system, but also sheds light on cue integration within decision-making processes. Yet, many significant phenomena across different fields lack clear explanations. For instance, in physiology, the integration mechanism of Drosophila's compass neuron when confronted with conflicting self-motion cues and external sensory cues with varying gain control settings is not well elucidated. Similarly, in ethology, the decision-making system shows Bayesian integration (BI) under minimal cue conflicts, but shifts to a winner-take-all (WTA) mode as conflicts surpass a certain threshold. To address these gaps, we introduce a ring attractor network with asymmetrical neural connections and synaptic dynamics in this paper. A thorough series of simulations has been conducted to assess its ability to track external cues and integrate conflicting cues. The results from these simulations demonstrate that the proposed model replicates observed neural dynamics and offers a framework for modeling biologically plausible cue integration behaviors. Furthermore, our findings yield several testable predictions that could inform future neuroethological research, providing insights into the role of ring attractor dynamics in the animal brain.

Supervised learning algorithm for analysis of communication signals in the weakly electric fish Apteronotus leptorhynchus

Signal analysis plays a preeminent role in neuroethological research. Traditionally, signal identification has been based on pre-defined signal (sub-)types, thus being subject to the investigator’s bias. To address this deficiency, we have developed a supervised learning algorithm for the detection of subtypes of chirps—frequency/amplitude modulations of the electric organ discharge that are generated predominantly during electric interactions of individuals of the weakly electric fish Apteronotus leptorhynchus. This machine learning paradigm can learn, from a ‘ground truth’ data set, a function that assigns proper outputs (here: time instances of chirps and associated chirp types) to inputs (here: time-series frequency and amplitude data). By employing this artificial intelligence approach, we have validated previous classifications of chirps into different types and shown that further differentiation into subtypes is possible. This demonstration of its superiority compared to traditional methods might serve as proof-of-principle of the suitability of the supervised machine learning paradigm for a broad range of signals to be analyzed in neuroethology.

Neuroethology in South America: past, present and future.

South America is a vast continent endowed with extraordinary biodiversity that offers abundant opportunities for neuroethological research. Although neuroethology is still emerging in the region, the number of research groups studying South American species to unveil the neural organization of natural behaviors has grown considerably during the last decade. In this Perspective, we provide an account of the roots and strategies that led to the present state of neuroethology in the Southern Cone of America, with a forward-looking vision of its role in education and its international recognition. Hopefully, our Perspective will serve to further promote the study of natural behaviors across South America, as well as in other scarcely explored regions of the world.

Neuroethology of sound localization in anurans.

Albert Feng pioneered the study of neuroethology of sound localization in anurans by combining behavioral experiments on phonotaxis with detailed investigations of neural processing of sound direction from the periphery to the central nervous system. The main advantage of these studies is that many species of female frogs readily perform phonotaxis towards loudspeakers emitting the species-specific advertisement call. Behavioral studies using synthetic calls can identify which parameters are important for phonotaxis and also quantify localization accuracy. Feng was the first to investigate binaural processing using single-unit recordings in the first two auditory nuclei in the central auditory pathway and later investigated the directional properties of auditory nerve fibers with free-field stimulation. These studies showed not only that the frog ear is inherently directional by virtue of acoustical coupling or crosstalk between the two eardrums, but also confirmed that there are extratympanic pathways that affect directionality in the low-frequency region of the frog's hearing range. Feng's recordings in the midbrain also showed that directional information is enhanced by cross-midline inhibition. An important contribution toward the end of his career involved his participation in neuroethological research with a team of scientists working with frogs that produce ultrasonic calls.

Doppler shift compensation performance in Hipposideros pratti across experimental paradigms

A central aim of neuroethological research is to discover the mechanisms of natural behaviors in controlled laboratory studies. This goal, however, comes with challenges, namely the selection of experimental paradigms that allow full expression of natural behaviors. Here, we explore this problem in echolocating bats that evolved Doppler shift compensation (DSC) of sonar vocalizations to yield close matching between echo frequency and hearing sensitivity. We ask if behavioral tasks influence the precision of DSC in Pratt’s roundleaf bat, Hipposideros pratti, in three classic laboratory paradigms evoking audio-vocal adjustments: Stationary bats listening to echo playbacks, bats transported on a moving pendulum, and bats flying freely. We found that experimental conditions had a strong influence on the expression of the audiovocal frequency adjustments in bats. H. pratti exhibited robust DSC in both free-flying and moving-pendulum experiments but did not exhibit consistent audiovocal adjustments in echo playback experiments. H. pratti featured a maximum compensation magnitude of 87% and a compensation precision of 0.27% in the free flight experiment. Interestingly, in the moving pendulum experiment H. pratti displayed surprisingly high-precision DSC, with an 84% maximum compensation magnitude and a 0.27% compensation precision. Such DSC performance places H. pratti among the bat species exhibiting the most precise audio-vocal control of echo frequency. These data support the emerging view that Hipposiderid bats have a high-precision DSC system and highlight the importance of selecting experimental paradigms that yield the expression of robust natural behaviors.

Interhemispheric Brain Communication and the Evolution of Turn-Taking in Mammals

In the last 20 years, research on turn-taking and duetting has flourished in at least three, historically separate disciplines: animal behavior, language sciences, and music cognition. While different in scope and methods, all three ultimately share one goal—namely the understanding of timed interactions among conspecifics. In this perspective, we aim at connecting turn-taking and duetting across species from a neural perspective. While we are still far from a defined neuroethology of turn-taking, we argue that the human neuroscience of turn-taking and duetting can inform animal bioacoustics. For this, we focus on a particular concept, interhemispheric connectivity, and its main white-matter substrate, the corpus callosum. We provide an overview of the role of corpus callosum in human neuroscience and interactive music and speech. We hypothesize its mechanistic connection to turn-taking and duetting in our species, and a potential translational link to mammalian research. We conclude by illustrating empirical venues for neuroethological research of turn-taking and duetting in mammals.

The Intervening Touch of Mentality: Food Seeking in Frogs and Whitehead’s Philosophy of Organism

Abstract Prey-catching behavior (PCB) in frogs and toads has been the focus of intense neuroethological research from the mid-twentieth century to the present and epitomizes some major themes in science and philosophy during this period. It reflects the movement from simple reflexology to more complex views of instinctive behavior, but it also displays a neural reductionism that denies subjectivity and individual agency. The present article engages contemporary PCB research but provides a philosophically more promising picture of it based on Whitehead’s nonreductionist “philosophy of organism,” which proposes that the flow of events from stimulus to response in organisms of all kinds is mediated by “the intervening touch of mentality.” This approach resolves some basic mind-body and mind-nature issues that have long bedeviled modern philosophy and presents an image of a postmodern frog for a constructively postmodern science.

The Intervening Touch of Mentality

Prey-catching behavior (PCB) in frogs and toads has been the focus of intense neuroethological research from the mid-twentieth century to the present and epitomizes some major themes in science and philosophy during this period. It reflects the movement from simple reflexology to more complex views of instinctive behavior, but it also displays a neural reductionism that denies subjectivity and individual agency The present article engages contemporary PCB research but provides a philosophically more promising picture of it based on Whitehead's nonreductionist "philosophy of organism," which proposes that the flow of events from stimulus to response in organisms of all kinds is mediated by "the intervening touch of mentality " This approach resolves some basic mind-body and mind-nature issues that have long bedeviled modern philosophy and presents an image of a postmodern frog for a constructively postmodern science.

"Introduction to the special issue on neuroethology": Correction to Simmons and Moss (2019).

Reports an error in "Introduction to the special issue on neuroethology" by Cynthia F. Moss and Andrea M. Simmons (Behavioral Neuroscience, 2019[Jun], Vol 133[3], 265-266). In the original article, the order of authors was reversed. The correct order of authors is Andrea M. Simmons and Cynthia F. Moss. The online version of this article has been corrected. (The following abstract of the original article appeared in record 2019-29253-001.) This special issue highlights some recent advances in neuroethology based on research presented at the 13th International Congress of Neuroethology and associated satellite symposia in Brisbane, Australia, on July 15-20, 2018. The discipline of neuroethology combines methods and concepts from ethology with those from neurobiology to develop a comparative analysis of the mechanisms of behavior that takes into account a species' ecology and evolutionary history. In his 1951 book The Study of Instinct, Nobel Prize winner Niko Tinbergen called on ethologists and neurophysiologists to join forces to search for mechanisms of motivated behaviors. He used the term "ethophysiology" to describe this integrative research approach, which he felt was crucial for developing a full understanding of behavior in all its complexities. At that time, "the ethologists were as naive about the neurophysiological significance of their findings as the neurophysiologists were about the behavioral implications of theirs" (Hoyle, 1984, p. 371). To rectify these limitations and to move forward, some of the earliest neuroethological research focused on understanding cellular mechanisms underlying the ethological concepts of releasers (sign stimuli) and fixed action patterns in species such as locusts and toads (Ewert, 1980; Hoyle, 1984). The breadth of neuroethological research soon expanded to include many other species, particularly those with distinct sensory or motor specializations (echolocating bats, electric fish, barn owls; Ewert, Capranica, & Ingle, 1983), as well as to understand neural mechanisms of more "general" behaviors, such as learning, memory, navigation, and communication. Molecular genetic, anatomical, and computational approaches are also part of the neuroethologist's toolbox. (PsycINFO Database Record (c) 2019 APA, all rights reserved).

Introduction to the special issue on neuroethology.

This special issue highlights some recent advances in neuroethology based on research presented at the 13th International Congress of Neuroethology and associated satellite symposia in Brisbane, Australia, on July 15-20, 2018. The discipline of neuroethology combines methods and concepts from ethology with those from neurobiology to develop a comparative analysis of the mechanisms of behavior that takes into account a species' ecology and evolutionary history. In his 1951 book The Study of Instinct, Nobel Prize winner Niko Tinbergen called on ethologists and neurophysiologists to join forces to search for mechanisms of motivated behaviors. He used the term "ethophysiology" to describe this integrative research approach, which he felt was crucial for developing a full understanding of behavior in all its complexities. At that time, "the ethologists were as naive about the neurophysiological significance of their findings as the neurophysiologists were about the behavioral implications of theirs" (Hoyle, 1984, p. 371). To rectify these limitations and to move forward, some of the earliest neuroethological research focused on understanding cellular mechanisms underlying the ethological concepts of releasers (sign stimuli) and fixed action patterns in species such as locusts and toads (Ewert, 1980; Hoyle, 1984). The breadth of neuroethological research soon expanded to include many other species, particularly those with distinct sensory or motor specializations (echolocating bats, electric fish, barn owls; Ewert, Capranica, & Ingle, 1983), as well as to understand neural mechanisms of more "general" behaviors, such as learning, memory, navigation, and communication. Molecular genetic, anatomical, and computational approaches are also part of the neuroethologist's toolbox. (PsycINFO Database Record (c) 2019 APA, all rights reserved).

The use of MEMRI for monitoring central nervous system activity during intact insect walking

BackgroundMonitoring neuronal activity in the intact behaving animal is most desired in neuroethological research, yet it is rarely straightforward or even feasible. Here we present the use of manganese enhanced magnetic resonance imaging (MEMRI), a technique allowing monitoring the activity of an animal’s nervous system during specific behavioral patterns. Using MEMRI we were able to show activity in different ganglia of the central nervous system of intact locusts during walking. ResultsWe injected two groups of locusts with manganese, which serves as a magnetic contrast agent. One group was forced to walk on a treadmill for two hours, while the other was immobilized and served as a control. Subsequently, all animals were scanned in a T1 MRI protocol, and the accumulation of manganese in the neuronal tissues that were active during walking was demonstrated by comparing the scans of the two groups. Two neuronal sites showed significantly higher T1 signal in the walking locusts compared to the immobilized ones: the prothoracic ganglion, which locally controls the front legs, and the subesophageal ganglion, a head ganglion which takes part in initiation and maintenance of walking. ConclusionMEMRI is a potent, non-invasive technique for monitoring neuronal activity in intact locusts, and arthropods in general. Specifically, it provides a promising way for revealing the role of central and high-order neuronal structures in motor behaviors such as walking.

Brood hiding test: a new bioassay for behavioral and neuroethological ant research

We describe a new bioassay for behavioral and neuroethological ant research, the brood hiding test. A group of adult ants is taken out of the nest, confined together with brood and exposed to strong light. Ants may interact with brood, and, in particular, transport it to the provided shadowed area. The brood hiding test may be accompanied by administration of neuroactive compounds and/or by measurements of their levels in the brain and/or in specific brain structures. During pilot tests with workers of Formica polyctena the values of the score quantifying ant behavior were positively correlated with the group size.

How the Owl Tracks Its Prey

The structure of owls' ears enable them to rapidly spatially locate the origin of sounds that are literally as quiet as a mouse. Author Masakazu Konishi describes clever and elegant experimentation to discover owls' binaural hearing, while including beautiful infrared photography of owl flight. This Classic article was first published in the July–August 1973 issue, and is reprinted as part of American Scientist’s centennial year celebration. The author is widely recognized for his neuroethological research on prey capture auditory systems in owls and singing in songbirds.

Long-duration anesthetization of squid (Doryteuthis pealeii)

Cephalopods, and particularly squid, play a central role in marine ecosystems and are a prime model animal in neuroscience. Yet, the capability to investigate these animals in vivo has been hampered by the inability to sedate them beyond several minutes. Here, we describe methods to anesthetize Doryteuthis pealeii, the longfin squid, noninvasively for up to 5 h using a 0.15 mol magnesium chloride (MgCl2) seawater solution. Sedation was mild, rapid (<4 min), and the duration could be easily controlled by repeating anesthetic inductions. The sedation had no apparent effect on physiological evoked potentials recorded from nerve bundles within the statocyst system, suggesting the suitability of this solution as a sedating agent. This simple, long-duration anesthetic technique opens the possibility for longer in vivo investigations on this and related cephalopods, thus expanding potential neuroethological and ecophysiology research for a key marine invertebrate group.

Sleep, Learning, and Birdsong

Neuroethological research combines approaches derived from animal behavior and neurobiology to examine the neuronal mechanisms of behavior, often in the context of laboratory experiments on species chosen for particular adaptations. Typically, these species are not traditional laboratory animals yet they contribute greatly to a broad, evolutionarily diverse view of nervous system function. The surprising role of sleep in the vocal learning process of songbirds is one such example, described here. Juvenile zebra finches show sleep-dependent daytime fluctuations in their patterns of singing starting after their first exposure to tutor songs. Nighttime bursting activity in the vocal control song system also changes after the onset of tutoring, with the neuronal changes preceding the changes in objective behavior (daytime singing). After tutoring, the nighttime bursting increases and exhibits structure that depends on the particular tutor song, and the nighttime expression of these changes requires normal auditory feedback during daytime singing. These observations shed light on the information carried in neuronal activity during sleep and on the adaptive plastic mechanisms engaged during sleep. They suggest a new hypothesis of sensorimotor learning, whereby sensory memories act indirectly on sensorimotor feedback by modifying networks through plastic changes at night. Sleep may also contribute to adult song maintenance, with nighttime neuronal replay conveying information about songs produced during the day and possibly mediating daily changes in the structure of premotor bursts. Collectively, these insights contribute a comparative perspective to theories of sleep and memory, which also help to inform a developing understanding of how humans acquire and retain memories.

Interactions between environmental changes and brain plasticity in birds

Neurogenesis and neuronal recruitment occur in many vertebrates, including humans. Most of the new neurons die before reaching their destination. Those which survive migrate to various brain regions, replace older ones and connect to existing circuits. Evidence suggests that this replacement is related to acquisition of new information. Therefore, neuronal replacement can be seen as a form of brain plasticity that enables organisms to adjust to environmental changes. However, direct evidence of a causal link between replacement and learning remains elusive. Our hypothesis is that increased neuronal recruitment is associated with increase in memory load. Moreover, since neuronal recruitment is part of a turnover process, we assume that the same conditions that favor survival of some neurons induce the death of others. I present studies that investigated the effect of various behaviors and environmental conditions (food-hoarding, social change, reproductive cycle) on neuronal recruitment and survival in adult avian brains, and discuss how these phenomena relate to the life of animals. I offer a frame and rationale for comparing neuronal replacement in the adult brain, in order to uncover the pressures, rules, and mechanisms that govern its constant rejuvenation. The review emphasizes the importance of using various approaches (behavioral, anatomical, cellular and hormonal) in neuroethological research, and the need to study natural populations, in order to fully understand how neurogenesis and neuronal replacement contribute to life of animals. Finally, the review indicates to future directions and ends with the hope that a better understanding of adult neuronal replacement will lead to medical applications.

Convulsant activity and neurochemical alterations induced by a fraction obtained from fruit Averrhoa carambola (Oxalidaceae: Geraniales)

We obtained a neurotoxic fraction (AcTx) from star fruit ( Averrhoa carambola) and studied its effects on GABAergic and glutamatergic transmission systems. AcTx had no effect on GABA/glutamate uptake or release, or on glutamate binding. However, it specifically inhibited GABA binding in a concentration-dependent manner (IC 50 = 0.89 μM). Video-electroencephalogram recordings demonstrated that following cortical administration of AcTx, animals showed behavioral changes, including tonic-clonic seizures, evolving into status epilepticus, accompanied by cortical epileptiform activity. Chemical characterization of AcTx showed that this compound is a nonproteic molecule with a molecular weight less than 500, differing from oxalic acid. This neurotoxic fraction of star fruit may be considered a new tool for neurochemical and neuroethological research.

Spatiotemporal properties of the BOLD response in the songbirds' auditory circuit during a variety of listening tasks

Auditory fMRI in humans has recently received increasing attention from cognitive neuroscientists as a tool to understand mental processing of learned acoustic sequences and analyzing speech recognition and development of musical skills. The present study introduces this tool in a well-documented animal model for vocal learning, the songbird, and provides fundamental insight in the main technical issues associated with auditory fMRI in these songbirds. Stimulation protocols with various listening tasks lead to appropriate activation of successive relays in the songbirds' auditory pathway. The elicited BOLD response is also region and stimulus specific, and its temporal aspects provide accurate measures of the changes in brain physiology induced by the acoustic stimuli. Extensive repetition of an identical stimulus does not lead to habituation of the response in the primary or secondary telencephalic auditory regions of anesthetized subjects. The BOLD signal intensity changes during a stimulation and subsequent rest period have a very specific time course which shows a remarkable resemblance to auditory evoked BOLD responses commonly observed in human subjects. This observation indicates that auditory fMRI in the songbird may establish a link between auditory related neuro-imaging studies done in humans and the large body of neuro-ethological research on song learning and neuro-plasticity performed in songbirds.

Effect of Ecological Pressures on Brains: Examples from Avian Neuroethology and General Meanings

Abstract Comparative neuroethological research emphasizes that brains of animals have been shaped by the specific demands and constraints imposed by the ecological niche that a species occupies. Since avian species have developed very diverse life styles and occupy extreme ecological niches, bird brains should show many specializations, which may be revealed in species that have survived under high ecological pressures. In this paper, we will give several examples of adaptations, in which we are able to correlate structural and physiological spe­cializations to the specific ecological demands: adaptations found to nocturnal hunting in barn owls, the characteristics of bird song and its underlying neurobiological correlates, retinopetal projections and their relation to peripheral attentional switching, looming detection, and adaptations related to memory capacities of food-storing birds. We stress especially that the analysis of the animal’s ecological situation is important in understanding the factors that shaped both behavior and the neuronal substrate.

Nerve Cells and Insect Behavior—Studies on Crickets

Intraspecific acoustic communication during pair formation in crickets provides excellent material for neuroethological research. It permits analysis of a distinct behavior at its neuronal level. This top-down approach considers first the behavior in quantitative terms, then searches for its computational rules (algorithms), and finally for neuronal implementations. The research described involves high resolution behavioral measurements, extra- and intracellular recordings, and marking and photoinactivation of single nerve cells. The research focuses on sound production in male and phonotactic behavior in female crickets and its underlying neuronal basis. Segmental and plurisegmental organization within the nervous system are examined as well as the validity of the single identified neuron approach. Neuroethological concepts such as central pattern generation, feedback control, command neuron, and in particular, cellular correlates for sign stimuli used in conspecific song recognition and sound source localization are discussed. Crickets are ideal insects for analyzing behavioral plasticity and the contributing nerve cells. This research continues and extends the pioneering studies of the late Kenneth David Roeder on nerve cells and insect behavior by developing new techniques in behavioral and single cell analysis.