Special Issue "Behavioural Methods to Study Cognitive Capacities of Animals"

A special issue of Animals (ISSN 2076-2615). This special issue belongs to the section "Human-Animal Interactions, Animal Behaviour and Emotion".

Deadline for manuscript submissions: 30 September 2021.

Special Issue Editors

Prof. Dr. Lucia Regolin
E-Mail Website
Guest Editor
Department of General Psychology, University of Padova, Padova, Italy
Interests: animal cognition; comparative psychology; domestic chicken (Gallus gallus)
Dr. Maria Loconsole
E-Mail Website
Guest Editor
Department of General Psychology, University of Padova, Padova, Italy
Interests: animal cognition; comparative psychology; domestic chicken (Gallus gallus)

Special Issue Information

Dear Colleagues,

Over the past 20 years, the scientific community has witnessed a growing interest in the comparative study of mental capabilities. Animal cognition has become an independent field of inter-disciplinary investigation, featuring specialized methodologies and paradigms tailored on diverse animal models. Recently, new approaches have emerged, offering access to large amounts of highly reliable data and to an enhanced explicatory power, at the cost of over-simplifying the behavioral response. On one hand are the automated and observer-independent techniques, which allow the collection of vast sets of data but may incur the risk of denaturing the meaning and richness of natural behaviors; on the other hand is the study of the neurobiological correlates of mental processes, which requires reference to standardized paradigms, posing constraints on the complexity and ecological validity of behavior. In contrast to these approaches, more traditional behavioral methods are firmly grounded on species’ ethology, considered crucial to grasp the distinctive qualitative features of the behavioral repertoire.

The present Special Issue aims at offering a collection of contributions employing behavioral methods to investigate the mental abilities of animals or any other behaving organism. Studies focusing on species’ natural behavior or comparing behavioral methods with other methodologies are also welcome.

Prof. Dr. Lucia Regolin
Dr. Maria Loconsole
Guest Editors

Manuscript Submission Information

Manuscripts should be submitted online at www.mdpi.com by registering and logging in to this website. Once you are registered, click here to go to the submission form. Manuscripts can be submitted until the deadline. All papers will be peer-reviewed. Accepted papers will be published continuously in the journal (as soon as accepted) and will be listed together on the special issue website. Research articles, review articles as well as short communications are invited. For planned papers, a title and short abstract (about 100 words) can be sent to the Editorial Office for announcement on this website.

Submitted manuscripts should not have been published previously, nor be under consideration for publication elsewhere (except conference proceedings papers). All manuscripts are thoroughly refereed through a single-blind peer-review process. A guide for authors and other relevant information for submission of manuscripts is available on the Instructions for Authors page. Animals is an international peer-reviewed open access monthly journal published by MDPI.

Please visit the Instructions for Authors page before submitting a manuscript. The Article Processing Charge (APC) for publication in this open access journal is 1800 CHF (Swiss Francs). Submitted papers should be well formatted and use good English. Authors may use MDPI's English editing service prior to publication or during author revisions.

Keywords

  • Animal cognition
  • Animal mind
  • Behavioral paradigms
  • Cognitive ethology
  • Comparative psychology
  • Animal intelligence

Published Papers (5 papers)

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Research

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Article
Carrion Crows and Azure-Winged Magpies Show No Prosocial Tendencies When Tested in a Token Transfer Paradigm
Animals 2021, 11(6), 1526; https://doi.org/10.3390/ani11061526 - 24 May 2021
Viewed by 398
Abstract
To study the evolution of humans’ cooperative nature, researchers have recently sought comparisons with other species. Studies investigating corvids, for example, showed that carrion crows and azure-winged magpies delivered food to group members when tested in naturalistic or simple experimental paradigms. Here, we [...] Read more.
To study the evolution of humans’ cooperative nature, researchers have recently sought comparisons with other species. Studies investigating corvids, for example, showed that carrion crows and azure-winged magpies delivered food to group members when tested in naturalistic or simple experimental paradigms. Here, we investigated whether we could replicate these positive findings when testing the same two species in a token transfer paradigm. After training the birds to exchange tokens with an experimenter for food rewards, we tested whether they would also transfer tokens to other birds, when they did not have the opportunity to exchange the tokens themselves. To control for the effects of motivation, and of social or stimulus enhancement, we tested each individual in three additional control conditions. We witnessed very few attempts and/or successful token transfers, and those few instances did not occur more frequently in the test condition than in the controls, which would suggest that the birds lack prosocial tendencies. Alternatively, we propose that this absence of prosociality may stem from the artificial nature and cognitive complexity of the token transfer task. Consequently, our findings highlight the strong impact of methodology on animals’ capability to exhibit prosocial tendencies and stress the importance of comparing multiple experimental paradigms. Full article
(This article belongs to the Special Issue Behavioural Methods to Study Cognitive Capacities of Animals)
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Article
Exploring the Cognitive Capacities of Japanese Macaques in a Cooperation Game
Animals 2021, 11(6), 1497; https://doi.org/10.3390/ani11061497 - 21 May 2021
Viewed by 450
Abstract
Cooperation occurs amongst individuals embedded in a social environment. Consequently, cooperative interactions involve a variety of persistent social influences such as the dynamics of partner choice and reward division. To test for the effects of such dynamics, we conducted cooperation experiments in a [...] Read more.
Cooperation occurs amongst individuals embedded in a social environment. Consequently, cooperative interactions involve a variety of persistent social influences such as the dynamics of partner choice and reward division. To test for the effects of such dynamics, we conducted cooperation experiments in a captive population of Japanese macaques (Macaca fuscata, N = 164) using a modified version of the loose-string paradigm in an open-experiment design. We show that in addition to becoming more proficient cooperators over the course of the experiments, some of the macaques showed sensitivity to the presence of potential partners and adjusted their behavior accordingly. Furthermore, following an unequal reward division, individuals receiving a lesser reward were more likely to display aggressive and stress-related behaviors. Our experiments demonstrate that Japanese macaques have some understanding of the contingencies involved in cooperation as well as a sensitivity to the subsequent reward division suggestive of an aversion to inequity. Full article
(This article belongs to the Special Issue Behavioural Methods to Study Cognitive Capacities of Animals)
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Article
Can Dogs Limbo? Dogs’ Perception of Affordances for Negotiating an Opening
Animals 2021, 11(3), 620; https://doi.org/10.3390/ani11030620 - 26 Feb 2021
Viewed by 1813
Abstract
Very little research has focused on canines’ understanding of their own size, and their ability to apply this understanding to their surroundings. The current study tests domestic dogs’ judgment of their body size in relation to a changing environment in two novel experimental [...] Read more.
Very little research has focused on canines’ understanding of their own size, and their ability to apply this understanding to their surroundings. The current study tests domestic dogs’ judgment of their body size in relation to a changing environment in two novel experimental situations: when encountering an opening of decreasing height (Study 1) and when negotiating an opening when carrying a stick in their mouth (Study 2). We hypothesized that if dogs understand their own body size, they will accurately judge when an opening is too small for their body to fit through, showing longer latencies to approach the smaller openings and adjusting their body appropriately to get through—although this judgment may not extend to when their body size is effectively increased. In line with these hypotheses, we found that the latency for subjects to reach an aperture they could easily fit through was significantly shorter than to one which was almost too small to fit through. We also found that the order of subjects’ adjustments to negotiate an aperture was invariant across individuals, indicating that dogs’ perception of affordances to fit through an aperture is action-scaled. Preliminary results suggest that dogs’ approach behavior is different when a horizontal appendage is introduced, but that dogs were able to alter their behavior with experience. These results are consistent with the hypothesis that dogs understand their own body size and the affordances of their changing environment. Full article
(This article belongs to the Special Issue Behavioural Methods to Study Cognitive Capacities of Animals)
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Review

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Review
Context-Specific Habituation: A Review
Animals 2021, 11(6), 1767; https://doi.org/10.3390/ani11061767 (registering DOI) - 12 Jun 2021
Viewed by 220
Abstract
Habituation consists of the progressive response decrement to a repeated stimulation, a response decline that is not accounted for by sensory or motor fatigue. Together with sensitization, habituation has been traditionally considered to be a prototypical example of non-associative learning, being affected only [...] Read more.
Habituation consists of the progressive response decrement to a repeated stimulation, a response decline that is not accounted for by sensory or motor fatigue. Together with sensitization, habituation has been traditionally considered to be a prototypical example of non-associative learning, being affected only by the features of the stimulation, as for instance its intensity or frequency. However, despite this widespread belief, evidence exists showing that habituation can be specific to the context of the stimulation, thus suggesting that habituation can have an associative nature. Such an unexpected characteristic of habituation was in fact predicted by a theoretical model of associative learning proposed by Wagner in a series of works that appeared in the late 1970s. Here, we critically review the experimental data that since then have been accumulated in support of this hypothesis. What emerges from the literature is that context-specific habituation is common to several animal species and that the ability to form an association between the habituating stimulus and its context is independent of the complexity of the animal’s nervous system. Finally, context-specific habituation is observed for a variety of organism’s responses, ranging from visceral to motor and mental activities. Full article
(This article belongs to the Special Issue Behavioural Methods to Study Cognitive Capacities of Animals)
Review
The Challenge of Illusory Perception of Animals: The Impact of Methodological Variability in Cross-Species Investigation
Animals 2021, 11(6), 1618; https://doi.org/10.3390/ani11061618 - 30 May 2021
Viewed by 445
Abstract
Although we live on the same planet, there are countless different ways of seeing the surroundings that reflect the different individual experiences and selective pressures. In recent decades, visual illusions have been used in behavioural research to compare the perception between different vertebrate [...] Read more.
Although we live on the same planet, there are countless different ways of seeing the surroundings that reflect the different individual experiences and selective pressures. In recent decades, visual illusions have been used in behavioural research to compare the perception between different vertebrate species. The studies conducted so far have provided contradictory results, suggesting that the underlying perceptual mechanisms may differ across species. Besides the differentiation of the perceptual mechanisms, another explanation could be taken into account. Indeed, the different studies often used different methodologies that could have potentially introduced confounding factors. In fact, the possibility exists that the illusory perception is influenced by the different methodologies and the test design. Almost every study of this research field has been conducted in laboratories adopting two different methodological approaches: a spontaneous choice test or a training procedure. In the spontaneous choice test, a subject is presented with biologically relevant stimuli in an illusory context, whereas, in the training procedure, a subject has to undergo an extensive training during which neutral stimuli are associated with a biologically relevant reward. Here, we review the literature on this topic, highlighting both the relevance and the potential weaknesses of the different methodological approaches. Full article
(This article belongs to the Special Issue Behavioural Methods to Study Cognitive Capacities of Animals)
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Planned Papers

The below list represents only planned manuscripts. Some of these manuscripts have not been received by the Editorial Office yet. Papers submitted to MDPI journals are subject to peer-review.

Title: Invasive research on primates – time to turn the page?
Authors: Maria Padrell; Miquel Llorente; Federica Amici
Affiliation: Max Planck Institute for Evolutionary Anthropology & University of Leipzig
Abstract: Invasive research on primates has a long history. Although some invasive studies have allowed answering research questions that we could not have addressed with other methods, ethical concerns about the use of primates in invasive research are steadily increasing. In this review, we (i) discuss the main ethical issues that have been raised on invasive research on primates, (ii) provide a brief historical overview of previous attempts to reduce the use of primates in invasive research, (iii) discuss the legislative protection that is granted to primates around the world, with a special focus on the principles of the 3Rs, and (iv) analyze recent cognitive advances in the study of primates that speak against their use in invasive research. Based on this evidence, we suggest that the importance of a research question cannot alone justify invasive research on primates, and that non-invasive behavioural and experimental methods should be considered the only possible approach to the study of primates.

Title: Techniques to investigate metacontrol in pigeons
Authors: Martina Manns
Affiliation: Ruhr-Universitat Bochum, Germany

Title: “ManyBirds” – a multi-lab collaborative approach to avian cognitive research
Authors: Megan Lambert; Rachael Miller
Affiliation: University of Veterinary Medicine, Vienna, Austria Department of Psychology, University of Cambridge, UK
Abstract: Comparative cognitive research aims to investigate cognitive evolution by comparing performance in different species to understand how these abilities have evolved. Ideally, this requires large and diverse samples, however these can be difficult to obtain by single labs or institutions, leading to potential reproducibility and generalisation issues with small, less representative samples. We outline the necessary infrastructure for a multi-lab collaborative Open Science approach to provide new insights into the evolution of avian cognition through comparative studies, following the lead of exemplary ManyPrimates, ManyBabies and ManyDogs projects, which may also be useful for devising similar projects in other taxa.

Title: Context-specific habituation: A review
Authors: Andrea Dissegna; Massimo Turatto; Cinzia Chiandetti
Affiliation: University of Triest, Italy
Abstract: Habituation consists of the progressive response decrement to a repeated stimulation that is not accounted for by sensory or motor fatigue. Together with sensitization, habituation has been traditionally considered to be a prototypical example of non-associative learning, being affected only by the features of the stimulation, as for instance its intensity or frequency. However, despite this widespread belief, evidence exists that habituation to a given stimulus can be specific for the context in which it appears, thus suggesting that habituation can have an associative nature. Such unexpected characteristic of habituation is in fact predicted by a theoretical model of associative learning proposed by Wagner in a series of works that appeared in the late ’70s. Here, we review the experimental data that, since then, have been accumulated in support of this hypothesis. What emerges from the literature is that context-specific habituation is common to several animal species and that the ability to form an association between the habituating stimulus and its context is independent of the complexity of the animal’s nervous system. Finally, context-specific habituation is observed for a variety of the organism’s responses, ranging from visceral to motor and mental activities.

Title: An invitation to revisit some core aspects of the Ethology discipline
Authors: Nereida Bueno Guerra
Affiliation: Calle Universidad Comillas, 3/5. 28049 - Madrid
Abstract: Disciplines grow and empower themselves after periods in which their core concepts or their methodologies are subjected to discussion. Ethology is not an exception: the introduction of reciprocal altruism by Trivers; the controversy about how consciousness was defined, brought by Nagel; the four whys of Niko Tinbergen or the perils of anthropomorphism warned by Wynne are just some examples pinpointing relevant revolutionary momentum for the study of animal behaviour. Far from seen as threatens, this stop-think-propose process nurtured the potential and the extent of the discipline. Nowadays, the findings of sister areas of knowledge, such as the coined “plant intelligence”, and the development of technology, such as drones, big data analysis or neurobiology techniques, in a varying and networked world, may invite to rethink the scope and the basic principles of animal behaviour. This exercise of analysis may help in building a common and solid ground for the discipline’s advancement. In this article, following the principles of philosophy of science, I postulate that five core aspects should be revisited: common definitions, criteria for the selection of study species, umwelt, technology and open science.

Title: Enabling plants' behavioural analysis: a stereovision based approach to kinematics
Authors: Valentina Simonetti; Maria Bulgheroni; Silvia Guerra; Alessandro Peressotti; Francesca Peressotti; Walter Baccinelli; Francesco Ceccarini; Bianca Bonato; Quiran Wang; Umberto Castiello
Affiliation: 1AB.ACUS Bioengineering, Milan, Italy 2Dipartimento di Psicologia Generale, Università di Padova, Italy 3Dipartimento di Scienze Agroalimentari, Ambientali e Animali, Università degli studi di Udine, Udine, Italy. 4Dipartimento di Psicologia dello Sviluppo e della Socializzazione, Università degli studi di Padova, Padova, Italy
Abstract: In this article we advance a methodology for the study of goal directed movements in plants via kinematical analysis. The targeted movement is circumnutation. Circumnutation is a helical organ movement widespread among plants. It is variable due to a different magnitude of trajectory (amplitude) outlined by the organ tip, duration of one cycle (period), circular, elliptical, pendulum-like or irregular shape and clock- and counterclockwise direction of rotation. The acquisition setup consists of two cameras used to obtain a stereoscopic vision of each plant. Cameras switch to infrared recording mode for low light level condition, allowing continuous motion acquisition also during the night. A dedicated software enables semi-automatic tracking of key points of the plant and, using the stereoscopic setup, reconstructs the 3D trajectory of each key point along the whole movement. 3D trajectories of different points undergo a devoted processing to compute features suitable to describe plants movement (maximum speed, circumnutation center, circumnutation length, etc.) and specific aspects of climbing plants behavior. By using this method, our recent studies have uncovered new functions of circumnutation in plants’ life previously unknown.

Title: Learning by doing: distance, corners and length in rewarded geometric tasks by zebrafish (Danio rerio)
Authors: Greta Baratti; Angelo Rizzo; Valeria Anna Sovrano
Affiliation: CIMeC, Center for Mind/Brain Sciences, University of Trento, Rovereto, Italy School of Natural Sciences, University of Torino, Italy Department of Psychology and Cognitive Science, University of Trento, Rovereto, Italy
Abstract: Zebrafish spontaneously use distance and directional relationships among extended three-dimensional surfaces to reorient within the rectangular-shaped arena. However, they fail to take advantage of either an array of freestanding corners or an array of unequal-length surfaces to search for a hidden goal in spontaneous cued memory paradigm: in fact, zebrafish cannot use the information supplied by corners and length without some kind of rewarded training. The present study aimed, in a reference memory paradigm, to tease apart the geometric components characterizing a rectangular enclosure, thus by training zebrafish in fragmented layouts that provided differences in surface distance, corners, and length. Results showed that zebrafish easily learned to use both corners and length if subjected to a rewarded exit task, that was, by applying a training procedure over time. These findings suggest that zebrafish can represent all the geometrically informative parts of a rectangular-shaped arena under reference memory conditions. All together, they further pave the way to deepen the role of visual and nonvisual encoding of macrostructural boundaries in spatial learning by such a species, highlighting critical issues on the use of different behavioral paradigms (spontaneous choice conditions vs. training over time).

Title: Carrion crows and azure-winged magpies show no prosocial tendencies when tested in a token exchange paradigm
Authors: Lisa Horn; Jeroen S. Zewald; Thomas Bugnyar; Jorg J. M. Massen
Affiliation: Department of Behavioral and Cognitive Biology, University of Vienna, Austria Animal Ecology Group, Department of Biology, Utrecht University, Utrecht, Netherlands
Abstract: Recent studies investigating prosocial behavior in corvids showed that carrion crows and azure-winged magpies delivered food to group members when tested in naturalistic or simple experimental paradigms. Here, we investigated whether we could replicate these positive findings when testing the same two species in a token exchange paradigm. After training the birds to exchange tokens with an experimenter for food reward, we tested whether an individual would transfer tokens to other birds, when the individual itself did not have the opportunity to exchange the tokens anymore. To control for effects of motivation, social and stimulus enhancement, we tested each individual in three additional control conditions. Our results show that overall there were very few attempts and/or successful token transfers. Those few instances did not occur more frequently in the test condition than in the controls, which would suggest that carrion crows and azure-winged magpies lack prosocial tendencies. Alternatively, we propose that this absence of prosocial giving may stem from the artificial nature and cognitive complexity of the token exchange task. Consequently, our findings highlight the strong impact of methodology on whether animals are able to exhibit their prosocial tendencies, and stress the importance of comparing multiple experimental paradigms.

Title: Exploring the cognitive capacities of Japanese macaques in a cooperation game
Authors: Ryan Sigmundson; Mathieu Stribos; Roy Hammer; Julia Herzele; Lena S Pflüger; Jorg J M Massen
Affiliation: Department of Philosophy, University of Vienna, Universitätsstraße 7, 1010 Vienna, Austria Animal Ecology Group, Department of Biology, Utrecht University, Padualaan 8, 3584 CH Utrecht, the Netherlands Austrian Research Center for Primatology, Ossiach 16, 9570 Ossiach, Austria Department of Behavioral and Cognitive Biology, University of Vienna, Althanstrasse 14, 1090 Vienna, Austria
Abstract: Cooperation occurs not in a vacuum, but amongst individuals embedded in a social environment. The importance of this fact has until recent times been largely overlooked in animal cooperation studies, resulting in a body of research that tests cooperation in rather artificial contexts and subsequently undervalues the impact of persistent social factors. We conducted cooperation experiments in a population of Japanese macaques (Macaca fuscata) living under semi-naturalistic conditions using a modified version of the loose-string paradigm. All animals were allowed to freely approach and take part in the experiment, and rewards were released onto a central platform. This design served to achieve a higher level of ecological validity through retention of partner choice and reward division dynamics, while still being able to test the potential cognitive processes involved. We show that in addition to becoming more proficient cooperators over the course of the experiments, some of the macaques came to show sensitivity to the presence of potential partners and adjusted their behavior accordingly. Furthermore, following an unequal reward division, individuals receiving a lesser reward were more likely to display aggressive and stress behaviors. Our experiments demonstrate that Japanese macaques possess not only some sort of understanding of the contingencies involved in cooperation, but also sensitivity to the reward division that occurs thereafter, and importantly, that this can be tested in an ecologically valid context.

Title: The Use of Behavioral Methodology to Examine Novel Pain Processing
Authors: Tiffany Aguirre
Affiliation: Department of Psychology, LS 504, The University of Texas at Arlington, USA
Abstract: The increased realization of the complexity of pain processing has resulted in a significant effort to develop more advanced preclinical behavioral methodology. As the study of the sensory, emotional/motivational and cognitive dimensions of pain have evolved, the development of these more complex methodologies has reliably and successfully provided novel and valuable information. The more recent focus of preclinical behavioral methodologies centers on the manner in which pain impacts not only basic emotional and motivational systems, but also on the effect pain has on higher order cognitive functions such as attention, learning, memory and decision making. Therefore, the purpose of this paper is to discuss some of the approaches that have been used. By discussing behavioral methods such as the Place Escape/Avoidance Paradigm, 5-Choice Serial Reaction Time Task, Novel Object Recognition Task and the Rat Gambling Task, we aim for this review to serve as a guide for future studies assessing the alteration of cognitive functioning as a result of various types of pain.

Title: A Review of the Model/Rival (M/R) Technique Used in Behavioral Research
Authors: Irene M. Pepperberg
Affiliation: Department of Psychology, Harvard University, USA
Abstract: In this paper I will review the Model/Rival (M/R) technique that has been uses to establish interspecies communication with Grey parrots (Psittacus erithacus). I will describe the original format developed by Todt, the relationship to other forms of observational learning by researchers such as Bandura and Krashen, and the adaptations that I devised. I will describe how my students and I isolated the various components that constitute the technique and explain how each is necessary but how only the combination of all components is sufficient for successful implementation. I will briefly summarize the results of such implementation and how improper implementation can lead to failure. I will describe how the technique has been adapted for use with children with communicative learning disabilities and suggest that it might be implemented in other areas of research if adapted appropriately.

Title: Studying Visuo-motor Abilities in Insects: The Promises of Virtual Reality
Authors: Elisa Frasnelli
Affiliation: University of Lincoln. Joseph Banks Laboratories, Green Lane, Lincoln, Lincolnshire, UK
Abstract: Insects move in very complex environments, where they must confront many challenges: They need to stabilise their flight, avoid obstacles, navigate specific distances to find food resources, and smoothly land on them. Some insects like bees also learn about locations to visit them in successive foraging trips and to communicate this information to other foragers within their colony. In all these tasks, insects are guided by their vision and specifically by the so-called optic flow, i.e. their capability to infer the 3rd dimension of the world from the 2D images on their retina. Previous studies have investigated these visuo-motor abilities in the laboratory where insects were observed in arenas with static physical objects in it. Such experimental setups present some limitations as they do not allow to manipulate visual cues independently nor to create “impossible” situations where, for example, a stimulus is moving away or toward the animal. The close-loop Virtual Reality (VR) technique allows overcoming such limitations. By tracking the position of a free-flying insect and presenting it with visual stimuli on a monitor that change in real time as a function of the insect’s own movements, the VR creates to animals the illusion of objects located in the 3D space. In this paper, I present the advantages of such a technique in the study of visuo-motor abilities in free moving insects and discuss its promises in animal cognition research.

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