Through an animal's eye: the implications of diverse sensory systems in scientific experimentation.

'Accounting for the sensory abilities of animals is critical in experimental design.' No researcher would disagree with this statement, yet it is often the case that we inadvertently fall for anthropocentric biases and use ourselves as the reference point. This paper discusses the risks of adopting an anthropocentric view when working with non-human animals, and the unintended consequences this has on our experimental designs and results. To this aim, we provide general examples of anthropocentric bias from different fields of animal research, with a particular focus on animal cognition and behaviour, and lay out the potential consequences of adopting a human-based perspective. Knowledge of the sensory abilities, both in terms of similarities to humans and peculiarities of the investigated species, is crucial to ensure solid conclusions. A more careful consideration of the diverse sensory systems of animals would improve many scientific fields and enhance animal welfare in the laboratory.

Behavioural Methods to Study Cognitive Capacities of Animals.

Over the past 20 years, the scientific community has witnessed a growing interest in the comparative study of mental capabilities [...].

Crossmodal association between visual and acoustic cues in a tortoise (Testudo hermanni).

Humans spontaneously match information coming from different senses, in what we call crossmodal associations. For instance, high-pitched sounds are preferentially associated with small objects, and low-pitched sounds with larger ones. Although previous studies reported crossmodal associations in mammalian species, evidence for other taxa is scarce, hindering an evolutionary understanding of this phenomenon. Here, we provide evidence of pitch-size correspondence in a reptile, the tortoise Testudo hermanni. Tortoises showed a spontaneous preference to associate a small disc (i.e. visual information about size) with a high-pitch sound (i.e. auditory information) and a larger disc to a low-pitched sound. These results suggest that crossmodal associations may be an evolutionary ancient phenomenon, potentially an organizing principle of the vertebrate brain.

Here I am, why don't you answer me? Sensitivity to social responsiveness in domestic chicks.

Newborn domestic chicks shortly exposed to a conspecific learn to recognize and prefer it over unfamiliar individuals. We assessed whether lack of physical contact or social feedback during familiarization affects affiliative preference, hypothesizing a crucial role of social responsiveness. Four-day-old chicks were tested for their preference between a familiar and an unfamiliar chick. In Exp. 1, we replicated the well-known preference for the familiar individual, even when (Exp. 2) a transparent glass prevented haptic interaction during familiarization. No preference was scored in Exp. 3, using a one-way glass, i.e., the subject could never be seen by its cagemate. The development of preferences toward a familiar but socially unresponsive cagemate was assessed by testing chicks twice (Exp. 4). While behaving at chance on day 2, birds showed a preference for the unfamiliar individual on day 4 of life. Our results highlight the importance of social interaction already in the first stages of life, irrespective of familiarity.

Processing Individually Distinctive Schematic-Faces Supports Proto-Arithmetical Counting in the Young Domestic Chicken.

A key signature of small-number processing is the difficulty in discriminating between three and four objects, as reported in infants and animals. Five-day-old chicks overcome this limit if individually distinctive features characterize each object. In this study, we have investigated whether processing individually different face-like objects can also support discrimination between three and four objects. Chicks were reared with seven face-like stimuli and tested in the proto-arithmetic comparison 1 + 1 + 1 vs. 1 + 1 + 1 + 1. Birds reared and tested with all different faces discriminated and approached the larger group (Exp. 1), whereas new birds reared and tested with seven identical copies of one same face failed (Exp. 2). The presence at test of individually different faces allowed discrimination even when chicks were reared with copies of one face (Exp. 3). To clarify the role of the previous experience of at least one specific arrangement of facial features, in Experiment 4, featureless faces were employed during rearing. During testing, chicks were unable to discriminate between three and four individually distinct faces. Results highlight the importance of having experienced at least one "face" in prompting individual processing and proto-arithmetical calculation later during testing. We speculate that mechanisms effective at the non-symbolic level may positively affect numerical performance.

Pitch-Luminance Crossmodal Correspondence in the Baby Chick: An Investigation on Predisposed and Learned Processes.

Our senses are constantly reached by a multitude of stimuli from all different sensory modalities. To create a coherent representation of the environment, we must integrate the various unimodal inputs that refer to the same object into a single multimodal representation. In some cases, however, we tend to bind certain properties of the stimuli without any apparent reason, which is a phenomenon named crossmodal correspondence. For instance, we match a spiky or a rounded shape with the sound "Kiki" or "Bouba", respectively. Similarly, we associate the left hemispace with low luminance and the right one with high luminance. Instances of crossmodal correspondences were described also in other mammals, and recently, a case of space-luminance crossmodal correspondence was reported in birds (i.e., domestic chicks). Here, we investigate the presence of pitch-luminance crossmodal correspondence in three-day-old chicks, employing experimental methods that exploit either predisposed or learned processes. While failing to report evidence for this phenomenon, we discuss the difference between statistical and structural crossmodal correspondences and the possible role of environmental factors in determining their emergence. Moreover, we discuss the importance of the different experimental methodologies to investigate distinct aspects of this perceptual phenomenon to reach a deeper understanding and unveil the role of innate vs. learned mechanisms.

Are prime numbers special? Insights from the life sciences.

Prime numbers have been attracting the interest of scientists since the first formulation of Euclid's theorem in 300 B.C. Nowadays, physicists and mathematicians continue to formulate new theorems about prime numbers, trying to comprehensively explain their articulated properties. However, evidence from biology and experimental psychology suggest that prime numbers possess distinctive natural properties that pre-exist human grasping. The present work aims at reviewing the existing literature on prime numbers in the life sciences, including some recent experimental contributions employing newly hatched domestic chicks as animal model to test for spontaneous mechanisms allowing discrimination of primes from non-primes. Our overarching goal is that of discussing some instances of prime numbers in nature, with particular reference to their peculiar, non-mathematical, perceptual properties.

Young chicks rely on symmetry/asymmetry in perceptual grouping to discriminate sets of elements.

Grouping sets of elements into smaller, equal-sized, subsets constitutes a perceptual strategy employed by humans and other animals to enhance cognitive performance. Here, we show that day-old chicks can solve extremely complex numerical discriminations (Exp.1), and that their performance can be enhanced by the presence of symmetrical/asymmetrical colour grouping (Exp.2 versus Exp.3). Newborn chicks were habituated for 1 h to even numerosities (sets of elements presented on a screen) and then tested for their spontaneous choice among what for humans would be considered a prime and a non-prime odd numerosity. Chicks discriminated and preferred the prime over the composite set of elements irrespective of its relative magnitude (i.e. 7 versus 9 and 11 versus 9). We discuss this result in terms of novelty preference. By employing a more complex contrast (i.e. 13 versus 15), we investigated the limits of such a mechanism and showed that induced grouping positively affects chicks' performance. Our results suggest the existence of a spontaneous mechanism that enables chicks to create symmetrical (i.e. same-sized) subgroups of sets of elements. Chicks preferentially inspected numerosities for which same-sized grouping is never possible (i.e. the prime numerosity) rather than numerosities allowing for symmetrical grouping (i.e. composite).

Jays are sensitive to cognitive illusions.

Jays hide food caches, steal them from conspecifics and use tactics to minimize cache theft. Jays are sensitive to the content of their own caches, retrieving items depending on their preferences and the perishability of the cached item. Whether jays impose the same content sensitivity when they steal caches is less clear. We adapted the 'cups-and-balls' magic routine, creating a cognitive illusion to test whether jays are sensitive to the (i) content of hidden items and (ii) type of displacement. Subjects were presented with two conditions in which hidden food was consistent with their expectations; and two conditions in which food was manipulated to violate their expectations by switching their second preferred food for their preferred food (up-value) or vice versa (de-value). Subjects readily accepted food when it was consistent with their expectations but were more likely to re-inspect the baited cup and alternative cup when their expectations were violated. In the de-value condition, jays exhibited longer latencies to consume the food and often rejected it. Dominant subjects were more likely to reject the food, suggesting that social factors influence their responses to cognitive illusions. Using cognitive illusions offers innovative avenues for investigating the psychological constraints in diverse animal minds.

A leftward bias negatively correlated with performance is selectively displayed by domestic chicks during rule reversal (not acquisition).

In order to face a constantly changing environment, animals need to be able to update their knowledge of the world on the basis of new information. Often, this means to inhibit a previously acquired response and flexibly change their behaviour to produce a new response. Here, we measured such abilities in young domestic chicks, employing a Colour Reversal Learning Task. During the acquisition phase, 17 one-week-old male chicks had to learn to peck on one of two coloured boxes to obtain a food reward. After reaching criterion, chicks underwent a reversal phase in which the previously learned colour-reward contingency was swapped. As expected from the literature, chicks performed better in the acquisition phase with respect to the reversal phase. Results moreover highlighted the presence of a lateralized bias selectively during reversal: chicks performed better if the stimulus rewarded was located in the left hemispace (processed by the right hemisphere). Interestingly, the bias correlated with the individual difficulty, i.e., it was stronger in those chicks which needed more trials to complete the reversal session. The present study contributes evidence in support of behavioural flexibility in young chicks, along with a novel perspective on lateralized mechanisms that might underlie such ability.

Individually distinctive features facilitate numerical discrimination of sets of objects in domestic chicks.

Day-old domestic chicks approach the larger of two groups of identical objects, but in a 3 vs 4 comparison, their performance is random. Here we investigated whether adding individually distinctive features to each object would facilitate such discrimination. Chicks reared with 7 objects were presented with the operation 1 + 1 + 1 vs 1 + 1 + 1 + 1. When objects were all identical, chicks performed randomly, as expected (Experiment 1). In the remaining experiments, objects differed from one another due to additional features. Chicks succeeded when those features were differently oriented segments (Experiment 2) but failed when the features were arranged to depict individually different face-like displays (Experiment 3). Discrimination was restored if the face-like stimuli were presented upside-down, disrupting global processing (Experiment 4). Our results support the claim that numerical discrimination in 3 vs 4 comparison benefits from the presence of distinctive features that enhance object individuation due to individual processing. Interestingly, when the distinctive features are arranged into upright face-like displays, the process is susceptible to global over local interference due to configural processing. This study was aimed at assessing whether individual object processing affects numerical discrimination. We hypothesise that in humans similar strategies aimed at improving performance at the non-symbolic level may have positive effects on symbolic mathematical abilities.

Multi-modal cue integration in the black garden ant.

In a constantly changing environment, it is advantageous for animals to encode a location (such as a food source) relying on more than one single cue. A certain position might, in fact, be signalled by the presence of information acquired through different sensory modalities which may be integrated into cohesive memories. Here, we aimed to investigate multi-sensory learning capabilities and multi-modal information integration in Lasius niger ants. Individual ants were placed in a Y-maze where odour information always led to a food reward; moreover, arm and wall colour were also predictive but only when co-occurring with odour in a specific combination. At test, the odour cue was made uninformative (it was present in both arms). Ants were still able to correctly locate the reward by integrating odour with the right colour and side combination. In a second experiment, we tested whether multi-modal cue integration can take place in a single trial. To this end, ants were exposed to a rewarded odour in a single-arm maze and could experience the Y-maze (with all available cues) only once. At test (which was identical to that of Experiment 1), ants showed a slight preference for the correct colour-side combination, although not significantly different from chance level. Our results showed the capability of black garden ants to code apparently redundant contextual information and to create and rely on conditional relationships between the information available. We argue that future studies should deepen the inquiry on the timing and progression of multi-modal cue learning.

Neurons in the Endbrain of Numerically Naive Crows Spontaneously Encode Visual Numerosity.

Endowed with an elaborate cerebral cortex, humans and other primates can assess the number of items in a set, or numerosity, from birth on [1] and without being trained [2]. Whether spontaneous numerosity extraction is a unique feat of the mammalian cerebral cortex [3-7] or rather an adaptive property that can be found in differently designed and independently evolved neural substrates, such as the avian enbrain [8], is unknown. To address this question, we recorded single-cell activity from the nidopallium caudolaterale (NCL), a high-level avian association brain area [9-11], of numerically naive crows. We found that a proportion of NCL neurons were spontaneously responsive to numerosity and tuned to the number of items, even though the crows were never trained to assess numerical quantity. Our data show that numerosity-selective neuronal responses are spontaneously present in the distinct endbrains of diverge vertebrate taxa. This seemingly hard-wired property of the avian endbrain to extract numerical quantity explains how birds in the wild, or right after hatching, can exploit numerical cues when making foraging or social decisions. It suggests that endbrain circuitries that evolved based on convergent evolution, such as the avian endbrain, give rise to the same numerosity code.

A strategy to improve arithmetical performance in four day-old domestic chicks (Gallus gallus).

A large body of literature shows that non-human animals master numerical discriminations, but a limit has been reported in a variety of species in the comparison 3vs.4. Little is known regarding the possibility of using "cognitive strategies" to enable this discrimination. The aims of this study were to investigate: whether domestic chicks discriminated 3vs.4, and if changes in stimuli presentation could improve chicks' numerical performance. Newly hatched chicks were reared with seven identical objects. On day 4, they underwent 20 consecutive testing trials to assess their capability to discriminate 3vs.4. The objects were presented, one-by-one, to the chicks and hidden behind one of two identical panels. As expected, the chicks did not discriminate (Experiment 1). When objects were presented and hidden in groups comprising one or two objects (2 + 1)vs.(2 + 2), the chicks succeeded (Experiment 2). The grouping strategy did not help in the case of a harder discrimination of (3 + 1)vs.(3 + 2) (Experiment 3), unless chicks were allowed to rest for two hours between testing sessions (Experiment 4). Our results suggest that in some cases, the limits reported for numerical performance in animals do not depend on cognitive limitations but on attentional or motivational factors, which can be overcome employing simple procedural adjustments.