Chunking as a function of sequence length.

Chunking mechanisms are central to several cognitive processes. During the acquisition of visuo-motor sequences, it is commonly reported that these sequences are segmented into chunks leading to more fluid, rapid, and accurate performances. The question of a chunk's storage capacity has been often investigated but little is known about the dynamics of chunk size evolution relative to sequence length. In two experiments, we studied the dynamics and the evolution of a sequence's chunking pattern as a function of sequence length in a non-human primate species (Guinea baboons, Papio papio). Using an operant conditioning device, baboons had to point on a touch screen to a moving target. In Experiment 1, they had to produce repeatedly the same sequence of 4 movements during 2000 trials. In Experiment 2, the sequence was composed of 5 movements and was repeated 4000 times. For both lengths, baboons initially produced small chunks that became fewer and longer with practice. Moreover, the dynamics and the evolution of the chunking pattern varied as a function of sequence length. Finally, with extended practice (i.e., more than 2000 trials), we observed that the mean chunk size reached a plateau indicating that there are fundamental limits to chunking processes that also depend on sequence length. These data therefore provide new empirical evidence for understanding the general properties of chunking mechanisms in sequence learning.

Humans (Homo sapiens) but not baboons (Papio papio) demonstrate crossmodal pitch-luminance correspondence.

Humans spontaneously and consistently map information coming from different sensory modalities. Surprisingly, the phylogenetic origin of such cross-modal correspondences has been under-investigated. A notable exception is the study of Ludwig et al. (Visuoauditory mappings between high luminance and high pitch are shared by chimpanzees [Pan troglodytes] and humans. Proceedings of the National Academy of Sciences, 108(51), 20661-20665) which reports that both humans and chimpanzees spontaneously map high-pitched sounds with bright objects and low-pitched sounds with dark objects. Our pre-registered study aimed to directly replicate this research on both humans and baboons (Papio papio), an old world monkey which is more phylogenetically distant from humans than chimpanzees. Following Ludwig et al. participants were presented with a visual classification task where they had to sort black and white square (low and high luminance), while background sounds (low or high-pitched tones) were playing. Whereas we replicated the finding that humans' performance on the visual task was affected by congruency between sound and luminance of the target, we did not find any of those effects on baboons' performance. These results question the presence of a shared cross-modal pitch-luminance mapping in other nonhuman primates.

Sensitivity to geometric shape regularity in humans and baboons: A putative signature of human singularity.

Among primates, humans are special in their ability to create and manipulate highly elaborate structures of language, mathematics, and music. Here we show that this sensitivity to abstract structure is already present in a much simpler domain: the visual perception of regular geometric shapes such as squares, rectangles, and parallelograms. We asked human subjects to detect an intruder shape among six quadrilaterals. Although the intruder was always defined by an identical amount of displacement of a single vertex, the results revealed a geometric regularity effect: detection was considerably easier when either the base shape or the intruder was a regular figure comprising right angles, parallelism, or symmetry rather than a more irregular shape. This effect was replicated in several tasks and in all human populations tested, including uneducated Himba adults and French kindergartners. Baboons, however, showed no such geometric regularity effect, even after extensive training. Baboon behavior was captured by convolutional neural networks (CNNs), but neither CNNs nor a variational autoencoder captured the human geometric regularity effect. However, a symbolic model, based on exact properties of Euclidean geometry, closely fitted human behavior. Our results indicate that the human propensity for symbolic abstraction permeates even elementary shape perception. They suggest a putative signature of human singularity and provide a challenge for nonsymbolic models of human shape perception.

Associative learning accounts for recursive-structure generation in crows.

Recursive sequence generation (i.e., the ability to transfer recursive patterns to novel items) was recently reported in crows (Liao et al., 2022, Science Advances, 8[44], eabq3356). Here, we argue that although the reported data are certainly compatible with the recursion hypothesis, they can also be explained by other, much simpler mechanisms of associative learning.

Simultaneous learning of directional and non-directional stimulus relations in baboons (Papio papio).

While humans exposed to a sequential stimulus pairing A-B are commonly assumed to form a bidirectional mental relation between A and B, evidence that non-human animals can do so is limited. Careful examination of the animal literature suggests possible improvements in the test procedures used to probe such effects, notably measuring transfer effects on the learning of B-A pairings, rather than direct recall of A upon cuing with B. We developed such an experimental design and tested 20 Guinea baboons (Papio papio). Two pairings of visual shapes were trained (A1-B1, A2-B2) and testing was conducted in a reversed order, either with conserved pairings (B1-A1, B2-A2) or broken ones (B1-A2, B2-A1). We found baboons' immediate test performance to be above chance level for conserved pairings and below chance level for broken ones. Moreover, baboons needed less trials to learn conserved pairings compared to broken ones. These effects were apparent for both pairings on average, and separately for the best learned pairing. Baboons' responding on B-A trials was thus influenced by their previous A-B training. Performance level at the onset of testing, however, suggests that baboons did not respond in full accordance with the hypothesis of bidirectionality. To account for these data, we suggest that two competing types of relations were concomitantly encoded: a directional relation between A and B, which retains the sequential order experienced, and a non-directional relation, which retains only the co-occurrence of events, not their temporal order.

On the role of interference in sequence learning in Guinea baboons (Papio papio).

It is well established that decay and interference are the two main causes of forgetting. In the present study, we specifically focus on the impact of interference on memory forgetting. To do so, we tested Guinea baboons (Papio papio) on a visuo-motor adaptation of the Serial Reaction Time task in which a target sequence is repeated, and a random sequence is interposed between repetitions, a similar situation as the one used in the Hebb repetition paradigm. In this task, one three-item sequence, the repeated sequence, was presented every second trial and interleaved with random sequences. Interference was implemented by using random sequences containing one item that was also part of the repeated sequence. In a first condition, the overlapping item was located at the same position as the repeated sequence. In a second condition, the overlapping item was located at one of the two other positions. In a third condition, there was no overlap between repeated and random sequences. Contrary to previous findings, our results reveal similar learning slopes across all three conditions, suggesting that interference did not affect sequence learning in the conditions tested. Findings are discussed in the light of previous research on sequence learning and current models of memory and statistical learning.

Simple questions on simple associations: regularity extraction in non-human primates.

When human and non-human animals learn sequences, they manage to implicitly extract statistical regularities through associative learning mechanisms. In two experiments conducted with a non-human primate species (Guinea baboons, Papio papio), we addressed simple questions on the learning of simple AB associations appearing in longer noisy sequences. Using a serial reaction time task, we manipulated the position of AB within the sequence, such that it could be either fixed (by appearing always at the beginning, middle, or end of a four-element sequence; Experiment 1) or variable (Experiment 2). We also tested the effect of sequence length in Experiment 2 by comparing the performance on AB when it was presented at a variable position within a sequence of four or five elements. The slope of RTs from A to B was taken for each condition as a measurement of learning rate. While all conditions differed significantly from a no-regularity baseline, we found strong evidence that the learning rate did not differ between the conditions. These results indicate that regularity extraction is not impacted by the position of the regularity within a sequence and by the length of the sequence. These data provide novel general empirical constraints for modeling associative mechanisms in sequence learning.

Categorization of vocal and nonvocal stimuli in Guinea baboons (Papio papio).

Categorization of vocal sounds apart from other sounds is one of the key abilities in human voice processing, but whether this ability is present in other animals, particularly nonhuman primates, remains unclear. In the present study, 25 socially housed Guinea baboons (Papio papio) were tested on a vocal/nonvocal categorization task using Go/Nogo paradigm implemented on freely accessible automated learning devices. Three individuals from the group successfully learned to sort Grunt vocalizations from nonvocal sounds, and they generalized to new stimuli from the two categories, indicating that some baboons have the ability to develop open-ended categories in the auditory domain. Contrary to our hypothesis based on the human literature, these monkeys learned the nonvocal category faster than the Grunt category. Moreover, they failed to generalize their classification to new classes of conspecific vocalizations (wahoo, bark, yak, and copulation calls), and they categorized human vocalizations in the nonvocal category, suggesting that they had failed to represent the task as a vocal versus nonvocal categorization problem. Thus, our results do not confirm the existence of a separate perceptual category for conspecific vocalizations in baboons. Interestingly, the three successful baboons are the youngest of the group, with less training in visual tasks, which supports previous reports of age and learning history as crucial factors in auditory laboratory experiments.

Constraints on the lexicons of human languages have cognitive roots present in baboons (Papio papio).

Using a pattern extraction task, we show that baboons, like humans, have a learning bias that helps them discover connected patterns more easily than disconnected ones-i.e., they favor rules like "contains between 40% and 80% red" over rules like "contains around 30% red or 100% red." The task was made as similar as possible to a task previously run on humans, which was argued to reveal a bias that is responsible for shaping the lexicons of human languages, both content words (nouns and adjectives) and logical words (quantifiers). The current baboon result thus suggests that the cognitive roots responsible for regularities across the content and logical lexicons of human languages are present in a similar form in other species.

Computerized assessment of dominance hierarchy in baboons (Papio papio).

Dominance hierarchies are an important aspect of Primate social life, and there is an increasing need to develop new systems to collect social information automatically. The main goal of this research was to explore the possibility to infer the dominance hierarchy of a group of Guinea baboons (Papio papio) from the analysis of their spontaneous interactions with freely accessible automated learning devices for monkeys (ALDM, Fagot & Bonté Behavior Research Methods, 42, 507-516, 2010). Experiment 1 compared the dominance hierarchy obtained from conventional observations of agonistic behaviours to the one inferred from the analysis of automatically recorded supplanting behaviours within the ALDM workstations. The comparison, applied to three different datasets, shows that the dominance hierarchies obtained with the two methods are highly congruent (all rs ≥ 0.75). Experiment 2 investigated the experimental potential of inferring dominance hierarchy from ALDM testing. ALDM data previously published in Goujon and Fagot (Behavioural Brain Research, 247, 101-109, 2013) were re-analysed for that purpose. Results indicate that supplanting events within the workstations lead to a transient improvement of cognitive performance for the baboon supplanting its partners and that this improvement depends on the difference in rank between the two baboons. This study therefore opens new perspectives for cognitive studies conducted in a social context.

High-fidelity copying is not necessarily the key to cumulative cultural evolution: a study in monkeys and children.

The unique cumulative nature of human culture has often been explained by high-fidelity copying mechanisms found only in human social learning. However, transmission chain experiments in human and non-human primates suggest that cumulative cultural evolution (CCE) might not necessarily depend on high-fidelity copying after all. In this study, we test whether defining properties of CCE can emerge in a non-copying task. We performed transmission chain experiments in Guinea baboons and human children where individuals observed and produced visual patterns composed of four squares on touchscreen devices. In order to be rewarded, participants had to avoid touching squares that were touched by a previous participant. In other words, they were rewarded for innovation rather than copying. Results nevertheless exhibited fundamental properties of CCE: an increase over generations in task performance and the emergence of systematic structure. However, these properties arose from different mechanisms across species: children, unlike baboons, converged in behaviour over generations by copying specific patterns in a different location, thus introducing alternative copying mechanisms into the non-copying task. In children, prior biases towards specific shapes led to convergence in behaviour across chains, while baboon chains showed signs of lineage specificity. We conclude that CCE can result from mechanisms with varying degrees of fidelity in transmission and thus that high-fidelity copying is not necessarily the key to CCE.

The baboon: A model for the study of language evolution.

Comparative research on the origins of human language often focuses on a limited number of language-related cognitive functions or anatomical structures that are compared across species. The underlying assumption of this approach is that a single or a limited number of factors may crucially explain how language appeared in the human lineage. Another potentially fruitful approach is to consider human language as the result of a (unique) assemblage of multiple cognitive and anatomical components, some of which are present in other species. This paper is a first step in that direction. It focuses on the baboon, a non-human primate that has been studied extensively for years, including several brain, anatomical, cognitive and cultural dimensions that are involved in human language. This paper presents recent data collected on baboons regarding (1) a selection of domain-general cognitive functions that are core functions for language, (2) vocal production, (3) gestural production and cerebral lateralization, and (4) cumulative culture. In all these domains, it shows that the baboons share with humans many cognitive or brain mechanisms which are central for language. Because of the multidimensionality of the knowledge accumulated on the baboon, that species is an excellent nonhuman primate model for the study of the evolutionary origins of language.

Isolation and characterization of olfactory ecto-mesenchymal stem cells from eight mammalian genera.

BACKGROUND: Stem cell-based therapies are an attractive option to promote regeneration and repair defective tissues and organs. Thanks to their multipotency, high proliferation rate and the lack of major ethical limitations, "olfactory ecto-mesenchymal stem cells" (OE-MSCs) have been described as a promising candidate to treat a variety of damaged tissues. Easily accessible in the nasal cavity of most mammals, these cells are highly suitable for autologous cell-based therapies and do not face issues associated with other stem cells. However, their clinical use in humans and animals is limited due to a lack of preclinical studies on autologous transplantation and because no well-established methods currently exist to cultivate these cells. Here we evaluated the feasibility of collecting, purifying and amplifying OE-MSCs from different mammalian genera with the goal of promoting their interest in veterinary regenerative medicine. Biopsies of olfactory mucosa from eight mammalian genera (mouse, rat, rabbit, sheep, dog, horse, gray mouse lemur and macaque) were collected, using techniques derived from those previously used in humans and rats. The possibility of amplifying these cells and their stemness features and differentiation capability were then evaluated. RESULTS: Biopsies were successfully performed on olfactory mucosa without requiring the sacrifice of the donor animal, except mice. Cell populations were rapidly generated from olfactory mucosa explants. These cells displayed similar key features of their human counterparts: a fibroblastic morphology, a robust expression of nestin, an ability to form spheres and similar expression of surface markers (CD44, CD73). Moreover, most of them also exhibited high proliferation rates and clonogenicity with genus-specific properties. Finally, OE-MSCs also showed the ability to differentiate into mesodermal lineages. CONCLUSIONS: This article describes for the first time how millions of OE-MSCs can be quickly and easily obtained from different mammalian genera through protocols that are well-suited for autologous transplantations. Moreover, their multipotency makes them relevant to evaluate therapeutic application in a wide variety of tissue injury models. This study paves the way for the development of new fundamental and clinical studies based on OE-MSCs transplantation and suggests their interest in veterinary medicine.

The processing of positional information in a two-item sequence limits the emergence of symmetry in baboons (Papio papio), but not in humans (Homo sapiens).

When trained to associate Stimulus A to Stimulus B, humans can derive the untrained symmetrical B to A relation while nonhuman animals have much more difficulties. Urcuioli (2008, Journal of the Experimental Analysis of Behavior, 90, 257--282; 2015, Conductal, 3, 4--25) proposed that the apparent difficulty of animals in symmetry testing reflects their double encoding of the information on the stimuli (identity and relation) and their positional (i.e., spatial and temporal/ordinal) characteristics. This comparative study tested the emergence of symmetry in humans and baboons in a task in which the position of the stimuli was manipulated independently of their relation. Humans and baboons initially learned to associate pairs of visual shapes on a touch screen in a specific order. Three pairs of (A-B, C-D, and E-F) stimuli were used in training. After training, the two species were tested with the B-A, F-C, and E-D pairs. The B-A pairs preserved the association initially learned with A-B but reversed the positional information relative to training. The F-C pair neither preserved the association nor the positional information of the training pairs, and positional information were the only cues preserved in the E-D pair. Humans showed a response time advantage for B-A, suggesting symmetry, but also for E-D, suggesting that they also process positional information. In baboons, the advantage was found only for E-D, suggesting that they only process positional information. These results confirm that the processing of stimulus pairs differ between nonhuman animals to humans.

Emotion-Cognition Interaction in Nonhuman Primates: Cognitive Avoidance of Negative Stimuli in Baboons (Papio papio)

It is well established that emotion and cognition interact in humans, but such an interaction has not been extensively studied in nonhuman primates. We investigated whether emotional value can affect nonhuman primates' processing of stimuli that are only mentally represented, not visually available. In a short-term memory task, baboons memorized the location of two target squares of the same color, which were presented with a distractor of a different color. Through prior long-term conditioning, one of the two colors had acquired a negative valence. Subjects were slower and less accurate on the memory task when the targets were negative than when they were neutral. In contrast, subjects were faster and more accurate when the distractors were negative than when they were neutral. Some of these effects were modulated by individual differences in emotional disposition. Overall, the results reveal a pattern of cognitive avoidance of negative stimuli, and show that emotional value alters cognitive processing in baboons even when the stimuli are not physically present. This suggests that emotional influences on cognition are deeply rooted in evolutionary continuity.

Orthographic processing in animals: Implications for comparative psychologists.

Two recent studies have shown that pigeons and baboons can discriminate written English words from nonwords, and these findings were interpreted as demonstrating that orthographic processing is possible in absence of linguistic knowledge. Here, I emphasize a different idea, which is that these studies also inform comparative psychologists on the evolutionary history of statistical learning in nonhuman animals, and on its pervasiveness and flexibility.

Using Automated Learning Devices for Monkeys (ALDM) to study social networks.

Social network analysis has become a prominent tool to study animal social life, and there is an increasing need to develop new systems to collect social information automatically, systematically, and reliably. Here we explore the use of a freely accessible Automated Learning Device for Monkeys (ALDM) to collect such social information on a group of 22 captive baboons (Papio papio). We compared the social network obtained from the co-presence of the baboons in ten ALDM testing booths to the social network obtained through standard behavioral observation techniques. The results show that the co-presence network accurately reflects the social organization of the group, and also indicate under which conditions the co-presence network is most informative. In particular, the best correlation between the two networks was obtained with a minimum of 40 days of computer records and for individuals with at least 500 records per day. We also show through random permutation tests that the observed correlations go beyond what would be observed by simple synchronous activity, to reflect a preferential choice of closely located testing booths. The use of automatized cognitive testing therefore presents a new way of obtaining a large and regular amount of social information that is necessary to develop social network analysis. It also opens the possibility of studying dynamic changes in network structure with time and in relation to the cognitive performance of individuals.

Categorization does not promote symmetry in Guinea baboons (Papio papio).

Humans have the capacity to use stimuli interchangeably by forming equivalence classes, and this ability seems to be supported by our language system. According to Sidman and Tailby (Conditional discrimination vs. matching to sample: an expansion of the testing paradigm. J Exp Anal Behav 37:5-22, 1982), the formation of equivalence classes require that three relations are derived among the class members, and past experiments have shown that one of these relations, i.e., symmetry, corresponding to the ability to reverse a relation (if A â†’ B, then B â†’ A), is extremely difficult to obtain in non-human animals. Because language development and the ability to form equivalence classes both co-occur in children with an increased ability to form categories, the current study tested the idea that category learning might promote symmetry in a nonhuman primate species. In Experiment 1, twelve Guinea baboons (Papio papio) were trained to associate 60 pictures of bears and 60 pictures of cars to two category labels, before being tested in symmetry trials. In Experiment 2, symmetry was trained and tested by reversing the association order between labels and pictures, using a new set of stimuli. In both experiments, the baboons successfully demonstrated category discrimination, but had only a weak (though significant) tendency to respond in accordance with symmetry during test trials. Altogether, our results confirm that symmetry is inherently difficult in non-human animals. We discuss possible explanations for such a limitation and give reasons for thinking that the effects of categorization on symmetry should be further investigated.

Assessment of metacognitive monitoring and control in baboons (Papio papio).

Metacognition refers to the ability of an organism to evaluate its states of knowledge (metacognitive monitoring) and engage in appropriate information-seeking behaviors when a lack of knowledge is detected (metacognitive control). This study assessed metacognitive monitoring and control in three Guinea baboons (Papio papio). Monkeys were required to report on a touchscreen the location of two target stimuli that had previously appeared briefly on a grid. They could either respond directly or use a "Repeat" key providing an opportunity to repeat the target stimuli. In Experiment 1, the baboons used the Repeat key more frequently in difficult trials and transferred this use of the key to novel conditions. Two baboons showed higher accuracy when they declined using the key compared to Baseline trials in which the key was not available, suggesting accurate metacognitive monitoring judgments. The same two baboons were consistently faster at reporting the targets' locations after a repetition of the stimulus. In Experiment 2, the baboons had to choose between two Repeat keys, one for each target. Two baboons showed a preference for repeating the presentation of the less visible target, suggesting that they identified what information they lack. Overall, results support the hypothesis of metacognitive monitoring in baboons, and also provide limited evidence for metacognitive control. We propose that tests requiring subjects to choose between several metacognitive responses in computerized tasks provide a suitable new approach for studying targeted information-seeking behaviors in animals.

Object-specific and relational learning in pigeons.

Abstract or relational stimulus processing requires an organism to appreciate the interrelations between or among two or more stimuli (e.g., same or different, less than or greater than). In the current study, we explored the role of concrete and abstract information processing in pigeons performing a visual categorization task which could be solved by attending to either the specific objects presented or the relation among the objects. In Experiment 1, we gave pigeons three training phases in which we gradually increased the variability (that is, the number of object arrays) in the training set. In Experiment 2, we trained a second group of pigeons with an even larger number of object arrays from the outset. We found that, the larger the variability in the training exemplars, the lesser the pigeons' attention to object-specific information and the greater their attention to relational information; nevertheless, the contribution of object-specific information to categorization performance was never completely eliminated. This pervasive influence of object-specific information is not peculiar to animals, but has been observed in young children and human adults as well.