Nonverbal Animals Research Articles

Anthropofabrication and the redressing of memory: an embodied approach to comparative cognition.

On what basis do researchers posit that humans and other animals share cognitive capacities? We argue that such claims are not based on inherent, pre-existing similarities, but rather emerge through a two-step process, which we will call 'anthropofabrication'. In the initial stage, embodied action-based strategies and environmental context in human studies are ignored owing to the need for measurement and quantification. Consequently, cognitive terms become disconnected from the context to which we apply them, and human classificatory cognitive terms are transformed into broad explanatory terms, assumed to be 'species-neutral'. The second phase entails translating and applying these generalized explanatory terms to specific nonverbal animals in ways that serve to further cloak differences between animals and other species. Here, again, researchers selectively discard contextual information to facilitate the comparison with humans. To limit anthropofabrication, we should (re)acknowledge that cognitive abilities are not species-neutral and cannot be detached from embodied action, perception and their context of occurrence. We illustrate our points about anthropofabrication using the example of memory research. This article is part of the theme issue 'Minds in movement: embodied cognition in the age of artificial intelligence'.

Mapping the neuroethological signatures of pain, analgesia, and recovery in mice

Ongoing pain is driven by the activation and modulation of pain-sensing neurons, affecting physiology, motor function, and motivation to engage in certain behaviors. The complexity of the pain state has evaded a comprehensive definition, especially in non-verbal animals. Here, in mice, we used site-specific electrophysiology to define key time points corresponding to peripheral sensitivity in acute paw inflammation and chronic knee pain models. Using supervised and unsupervised machine learning tools, we uncovered sensory-evoked coping postures unique to each model. Through 3D pose analytics, we identified movement sequences that robustly represent different pain states and found that commonly used analgesics do not return an animal's behavior to a pre-injury state. Instead, these analgesics induce a novel set of spontaneous behaviors that are maintained even after resolution of evoked pain behaviors. Together, these findings reveal previously unidentified neuroethological signatures of pain and analgesia at heightened pain states and during recovery.

1-Back reinforcement symbolic-matching by humans: How do they learn it?

For humans, a distinction has been made between implicit and explicit learning. Implicit learning is thought to involve automatic processes of the kind involved in much Pavlovian conditioning, while explicit learning is thought to involve conscious hypothesis testing and rule formation, in which the subject's statement of the rule has been taken as evidence of explicit learning. Various methods have been used to determine if nonverbal animals are able to learn a task explicitly - among these is the 1-back reinforcement task in which feedback from performance on the current conditional discrimination trial is provided only after completion of the following trial. We propose that it is not whether an organism can learn the task, but whether they learn it rapidly, all-or-none, that provides a better distinction between the two kinds of learning. We had humans learn a symbolic matching, 1-back reinforcement task. Almost half of the subjects failed to learn the task, and of those who did, none described the 1-back rule. Thus, it is possible to learn this task without learning the 1-back rule. Furthermore, the backward learning functions for humans differ from those of pigeons. Human subjects who learned the task did so all-or-none, suggesting explicit learning. In earlier research with pigeons, they too showed significant learning of this task; however, backward learning functions suggested that they did so gradually over the course of several sessions of training and to a lower level of asymptotic accuracy than the humans, a result suggesting implicit learning was involved.

Current Understanding of the "Insight" Phenomenon Across Disciplines.

Despite countless anecdotes and the historical significance of insight as a problem solving mechanism, its nature has long remained elusive. The conscious experience of insight is notoriously difficult to trace in non-verbal animals. Although studying insight has presented a significant challenge even to neurobiology and psychology, human neuroimaging studies have cleared the theoretical landscape, as they have begun to reveal the underlying mechanisms. The study of insight in non-human animals has, in contrast, remained limited to innovative adjustments to experimental designs within the classical approach of judging cognitive processes in animals, based on task performance. This leaves no apparent possibility of ending debates from different interpretations emerging from conflicting schools of thought. We believe that comparative cognition has thus much to gain by embracing advances from neuroscience and human cognitive psychology. We will review literature on insight (mainly human) and discuss the consequences of these findings to comparative cognition.

OUTLINING A DIALOGUE BETWEEN SIDMAN AND HAYES ABOUT EMERGENT RELATIONS (1982-1994)

Stimulus equivalence, as presented by Sidman and his colleagues, and relational frame theory, proposed by Hayes and his colleagues, are two of the main alternatives for explaining emergent relations between stimuli. The goal of this study is to analyze Hayes’s criticisms of Sidman’s conceptual contributions and Sidman’s criticisms of Hayes’s conceptual contributions between 1982 and 1994. Hayes and colleagues deviated from Sidman and colleagues when the former argued the following: contingencies that are systematically arranged by a verbal community seem to be necessary for the emergence of stimulus equivalence; that Sidman’s concept of stimulus equivalence fails to explain why nonverbal animals are not capable to demonstrating equivalence; and that Sidman’s concept of stimulus equivalence is merely descriptive and lacks a theoretical explanation for the emergence of the phenomenon. In turn, Sidman confronted some of these issues and argued that relational frame theory is based on hypothetical generalized operant behaviors, without a simple explanation based on known behavioral principles and without the necessary supporting data. He pointed to the various experimental studies that should be carried out to tackle the divergences that had appeared.

1-Back reinforcement matching and mismatching by pigeons: Implicit or explicit learning?

In human learning a distinction has been made between implicit and explicit learning. Implicit learning is thought involve automatic processes of the kind involved in Pavlovian conditioning, while explicit learning is thought to involve conscious hypothesis testing and rule formation, in which the ability to report the rule used to learn the task is taken as evidence. Because non-verbal animals cannot provide such evidence, several indirect methods have been proposed. One of these methods is faster learning by humans of certain explicitly learned tasks than implicitly learned tasks, but pigeons do not show a similar difference. Another method involves the 1-back-reinforcement conditional discrimination (if A choose X, if B choose Y) in which feedback following the conditional response is delayed until the next trial. It has been argued that implicit learning cannot occur over the delay between the conditional response and the reinforcer on the next trial, yet, it has been found that monkeys can learn this 1-back reinforcement task. We have argued that such learning can occur implicitly. We have found that pigeons, a species not thought to learn explicitly, can show significant learning of both 1-back reinforcement matching and 1-back reinforcement mismatching, two versions of the 1-back-reinforcement conditional discrimination. We propose that the evidence for explicit learning by non-verbal animals suffers from alternative simpler accounts because the rationale for explicit learning is based on assumptions that likely are not correct.

Pigeons acquire the 1-back task: Implications for implicit versus explicit learning?

In humans, a distinction can be made between implicit or procedural learning (involving stimulus-response associations) and explicit or declarative learning (involving verbalizable rules) that is relatively easy to make in verbal humans. According to several investigators, it is also possible to make such a distinction in nonverbal animals. One way is by training them on a conditional discrimination task (e.g., matching-to-sample) in which reinforcement for correct choice on the current trial is delayed until after a choice is made on the next trial - a method known as the 1-back procedure. According to Smith, Jackson, and Church ( Journal of Comparative Psychology, 134(4), 423-434, 2020), the delay between the sample-correct-comparison response on one trial and reinforcement obtained on the next trial is too long for implicit (associative) learning. Thus, according to this theory, learning must be explicit. In the present experiments we trained pigeons using the 1-back procedure. In Experiment 1, pigeons were trained on red/green 1-back matching using a non-correction procedure. Some of the pigeons showed significant learning. When a correction procedure was introduced, all the pigeons showed evidence of learning. In Experiment 2, new pigeons learned red/green 1-back matching with the correction procedure. In Experiment 3, new pigeons learned symbolic 1-back matching with yellow and blue conditional stimuli and red/green choice stimuli. Thus, pigeons can learn using 1-back reinforcement. Although it would appear that the pigeons acquired this task explicitly, we believe that this procedure does not adequately distinguish between implicit and explicit learning.

Towards describing scenes by animals: Pigeons' ordinal discrimination of objects varying in depth.

The perception of a complex scene requires visual mechanisms that include identifying objects and their relative placement in depth. To examine apparent depth perception in birds, we tested four pigeons with a novel multiple-sequential-choice procedure. We created 3D-rendered scene stimuli containing three objects located at different apparent depths based on a variety of pictorial cues and placed small circular target response areas on them. The pigeons were trained to sequentially choose among the multiple response areas to report the object closest in apparent depth (ordinal position; front then middle object). After the pigeons learned this sequential depth discrimination, their use of three different monocular depth cues (occlusion, relative size, height in field) was tested, and their flexibility evaluated using three novel objects. In addition to the contribution to understanding apparent depth perception in birds, the use of more flexible open-ended choice discriminations, as employed here, has considerable promise for creating informative production-like tasks in nonverbal animals.

Reflections on the spoon test

In this paper, we shall use Tulving's seminal empirical and theoretical research including the ‘Spoon Test’ to explore memory and mental time travel and its origins and role in planning for the future. We will review the comparative research on future planning and episodic foresight in pre-verbal children and non-verbal animals to explore how this may be manifest as wordless thoughts.

Grooming, social rank and ‘optimism’ in tufted capuchin monkeys: a study of judgement bias

Studying the emotional consequences of social behaviour in nonverbal animals require methods to access their emotional state. One such method is provided by cognitive bias tests. We applied a judgement bias test to tufted capuchin monkeys, Sapajus sp., to evaluate (1) whether receiving grooming was associated with a short-term increase in ‘optimism’ (that is, a positive bias in the interpretation of ambiguous stimuli) and (2) whether interindividual differences in ‘optimism’ were related to dominance rank or overall rates of social and nonsocial behaviour. Receiving grooming had no detectable immediate consequences, but increased ‘optimism’ was observed in dominant monkeys and in monkeys that received overall larger quantities of grooming. These results provide only partial support for the hypothesis that a system of emotional bookkeeping underlies the capacity of group-living animals to reciprocate cooperative interactions.

Methods for measuring pain in laboratory animals.

Pain is one of the most important variables that members of the lab animal science community try to control and minimize, and it is a critical topic of research in clinical and basic sciences. Objective measurements of pain severity, especially in non-verbal animals that are used as disease models, can be difficult to obtain, but several developments in behavioral neuroscience are making the measurement of pain more consistent, automated and accurate.

Anhedonia in pigs? Effects of social stress and restraint stress on sucrose preference

The fact that consumption of normally palatable foods is affected by stress in both humans and rats suggests a means to assess hedonic reaction in non-verbal animals. However, little is known about anhedonia and stress in productive animals such as pigs. Thus we examined the separate effects of social stress and restraint stress in 42-day old pigs on the preference for dilute sucrose solutions over water. Pigs in the social stress group (SS) were mixed with unfamiliar animals from separate pens for two 20minute periods (Experiment 1). Pigs in the restraint stress group (RS) were immobilized three times a day, for 3-min periods, on 3 consecutive days (Experiment 2). Consumption of dilute sucrose solutions and water was examined after these stress manipulations and in the unstressed control groups (CG). Pigs were tested in pairs (12 control and 12 experimental) with a choice between water and sucrose solutions (at either 0.5% or 1%) during 30min sessions. In both experiments CG pigs showed higher intakes of 0.5% and 1% sucrose solutions over water. Neither SS nor RS pigs consumed more 0.5% sucrose than water, but both groups did consume more 1% sucrose than water. Both social stress and restraint stress reduced sucrose preference at low concentrations but not at higher concentrations suggesting that stress may limit food consumption in pigs unless a palatable feed is present. In addition, the results suggest that stress reduces the hedonic impact of dilute sucrose. Therefore, sucrose preference may be a useful test for the presence of stress and anhedonia in pigs.

Macaque cardiac physiology is sensitive to the valence of passively viewed sensory stimuli.

Autonomic nervous system activity is an important component of affective experience. We demonstrate in the rhesus monkey that both the sympathetic and parasympathetic branches of the autonomic nervous system respond differentially to the affective valence of passively viewed video stimuli. We recorded cardiac impedance and an electrocardiogram while adult macaques watched a series of 300 30-second videos that varied in their affective content. We found that sympathetic activity (as measured by cardiac pre-ejection period) increased and parasympathetic activity (as measured by respiratory sinus arrhythmia) decreased as video content changes from positive to negative. These findings parallel the relationship between autonomic nervous system responsivity and valence of stimuli in humans. Given the relationship between human cardiac physiology and affective processing, these findings suggest that macaque cardiac physiology may be an index of affect in nonverbal animals.

Evaluation of reward from pain relief

The human experience of pain is multidimensional and comprises sensory, affective, and cognitive dimensions. Preclinical assessment of pain has been largely focused on the sensory features that contribute to nociception. The affective (aversive) qualities of pain are clinically significant but have received relatively less mechanistic investigation in preclinical models. Recently, operant behaviors such as conditioned place preference, avoidance, escape from noxious stimulus, and analgesic drug self-administration have been used in rodents to evaluate affective aspects of pain. An important advance of such operant behaviors is that these approaches may allow the detection and mechanistic investigation of spontaneous neuropathic or ongoing inflammatory/nociceptive (i.e., nonevoked) pain that is otherwise difficult to assess in nonverbal animals. Operant measures may allow the identification of mechanisms that contribute differentially to reflexive hypersensitivity or to pain affect and may inform the decision to progress novel mechanisms to clinical trials for pain therapy. Additionally, operant behaviors may allow investigation of the poorly understood mechanisms and neural circuits underlying motivational aspects of pain and the reward of pain relief.

Mood and anxiety disorders in chimpanzees (pan troglodytes): A response to Rosati et al. (2012).

Assessing the psychological health of nonhuman primates living in captivity is essential, since many experiments and behavioral observations involve captive animals. This area is a research priority because it has ethical consequences, in addition to its applications for understanding human and nonhuman primate behavior. In 2011, we published our international study's findings that chimpanzees with prior histories of experimentation, orphanage, illegal seizure, or violent human conflict were more likely to display signs of mood and anxiety disorders, compared with chimpanzees living in the wild. Here, in response to Rosati and colleagues (2012), we address methodological challenges relevant to the application of human diagnostic psychiatric criteria to nonverbal animals. We also review the importance of understanding psychopathology using a holistic approach based on evolutionary psychiatry and suggest a way forward, integrating ethological, veterinary, and human psychiatric approaches.

Assessing the psychological health of captive and wild apes: A response to Ferdowsian et al. (2011).

As many studies of cognition and behavior involve captive animals, assessing any psychological impact of captive conditions is an important goal for comparative researchers. Ferdowsian and colleagues (2011) sought to address whether captive chimpanzees show elevated signs of psychopathology relative to wild apes. They modified a checklist of diagnostic criteria for major depression and posttraumatic stress disorder in humans, and applied these criteria to various captive and wild chimpanzee populations. We argue that measures derived from human diagnostic criteria are not a powerful tool for assessing the psychological health of nonverbal animals. In addition, we highlight certain methodological drawbacks of the specific approach used by Ferdowsian and colleagues (2011). We propose that research should (1) focus on objective behavioral criteria that account for species-typical behaviors and can be reliably identified across populations; (2) account for population differences in rearing history when comparing how current environment impacts psychological health in animals; and (3) focus on how changes in current human practices can improve the well-being of both captive and wild animals.

Licking and Liking: The Assessment of Hedonic Responses in Rodents

Affective processes are a key determinant of behaviour: At its simplest, liked stimuli are approached while disliked stimuli are avoided. Although assessing hedonic responses in nonverbal animals can be difficult, one relatively tractable approach relies on detailed analyses of rodents' consummatory behaviour. Rodents typically produce rhythmic sets of licks that can be grouped into clusters on the basis of the intervals between licks. The mean number of licks in a cluster (cluster size) is directly related to the concentration of palatable and unpalatable solutions. These relationships suggest that lick cluster size might be a useful index of an animal's hedonic reaction to the solution being consumed. I begin by reviewing studies of conditioned flavour preference and aversion that support the idea that lick cluster size can provide useful information about rats' hedonic reactions. I then describe how this methodology has been used to address previously intractable issues in the investigation of contrast effects as well as revealing an analogue of effort justification effects that, in humans, are commonly explained in terms of cognitive dissonance reduction. Finally, I consider how lick analysis might provide information about hedonic responses in animal models of human psychiatric disorders. In all these cases, how an animal did something was particularly informative about why it was doing it.

Compressed Scaling of Abstract Numerosity Representations in Adult Humans and Monkeys

There is general agreement that nonverbal animals and humans endowed with language possess an evolutionary precursor system for representing and comparing numerical values. However, whether nonverbal numerical representations in human and nonhuman primates are quantitatively similar and whether linear or logarithmic coding underlies such magnitude judgments in both species remain elusive. To resolve these issues, we tested the numerical discrimination performance of human subjects and two rhesus monkeys (Macaca mulatta) in an identical delayed match-to-numerosity task for a broad range of numerosities from 1 to 30. The results demonstrate a noisy nonverbal estimation system obeying Weber's Law in both species. With average Weber fractions in the range of 0.51 and 0.60, nonverbal numerosity discriminations in humans and monkeys showed similar precision. Moreover, the detailed analysis of the performance distributions exhibited nonlinearly compressed numerosity representations in both primate species. However, the difference between linear and logarithmic scaling was less pronounced in humans. This may indicate a gradual transformation of a logarithmic to linear magnitude scale in human adults as the result of a cultural transformation process during the course of mathematical education.

Discrimination of the larger shoal in the poeciliid fish Girardinus falcatus

Two decades of comparative studies have shown that numerical abilities are widespread in the animal kingdom. In particular, the ability to select the larger of two quantities (known as the ability to go for “more”) has been found in apes, dolphins, birds and amphibians. This primary quantity discrimination has not been investigated in fish in a systematic way although several studies suggest that fish have the ability to distinguish among different-sized groups of conspecifics. We investigated the spontaneous choice for the larger of two shoals in female goldbelly topminnows (Girardinus falcatus) and compared two different methods to determine an efficient procedure for studying the numerical competence of fish. Female topminnows that were placed in a novel and potentially dangerous environment were found to choose the larger shoal suggesting that the capacity to go for “more” was similar to that observed in other non-verbal animals. The two methods proved not to be sensitive in revealing differences between the numerical contrasts, however, combining the results of the two experiments, we found that when groups differed in size by one individual, choice of the larger shoal was significantly above that predicted by chance up to a maximum of three fish in the larger shoal (i.e. 2 vs 1 and 3 vs 2 but not 4 vs 3 or larger). When presented with two shoals with a 1:2 numerical ratio, choice was significantly above chance in 4 vs 2 but not in 8 vs 4 comparisons.

The multisensory representation of number in infancy

Human infants can discriminate visual and auditory stimuli solely on the basis of number, suggesting a developmental foundation for the nonverbal number representations of adult humans. Recent studies suggest that these language-independent number representations are multisensory in both adult humans and nonhuman animals. Surprisingly, however, previous studies have yielded mixed evidence concerning whether nonverbal numerical representations independent of sensory modality are present early in human development. In this article, we use a paradigm that avoids stimulus confounds present in previous studies of cross-modal numerical mapping in infants. We show that 7-month-old infants preferentially attend to visual displays of adult humans that numerically match the number of adult humans they hear speaking. These data provide evidence that by 7 months of age, infants connect numerical representations across different sensory modalities when presented with human faces and voices. Results support the possibility of a shared system between preverbal infants and nonverbal animals for representing number.