Do they know or just do it? Investigating implicit and explicit sequence learning by capuchin monkeys, human adults and children.

In humans, it is now established that sequential regularities can be learned implicitly (i.e. without acquiring conscious knowledge) or explicitly (with acquisition of conscious knowledge). Is this dual-processing capability also the case for non-human primates? In this study, we designed a non-verbal task to probe implicit and explicit sequence learning in capuchin monkeys (Sapajus sp., n = 12), human adults (n = 12), and children from 5 to 10 years old (n = 64). After learning spatial sequences on a touchscreen, participants' conscious access to the sequences was probed with a forced choice sequence completion test. All performed above chance level in this test, without being instructed or trained to do so. However, only human adults who reported the presence of regularities performed at ceiling level. We suggest future directions that could build on our findings to disentangle implicit and explicit learning in monkeys and children.

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.

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.

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.

Tufted capuchins (Cebus apella) adapt their communicative behaviour to human's attentional states.

Animal communication has become a widely studied field of research, especially because of the associated debates on the origin of human language. Due to their phylogenetic proximity with humans, non-human primates represent a suitable model to investigate the precursors of language. This study focuses on the perception of the attentional states of others, an important prerequisite to intentional communication. We investigated whether capuchins (Cebus apella) produce a learnt pointing gesture towards a hidden and unreachable food reward as a function of the attentional status of the human experimenter. For that purpose, we tested five subjects that we first trained to indicate by a pointing gesture towards the human partner the position of a reward hidden by an assistant. Then, capuchins were tested in two experimental conditions randomly ordered. In the first condition-motivation trial-the experimenter was attentive to the subject gestures and rewarded him immediately when it pointed towards the baited cylinder. During the second condition-test trial-the experimenter adopted one of the following attention states and the subject was rewarded after 10 s has elapsed, regardless of the subject's behaviour. Five attentional states were tested: (1) experimenter absent, (2) experimenter back to the monkey, (3) experimenter's head away, (4) experimenter watching above the monkey, and (5) experimenter watching the monkey face. Our results reveal a variation in our subjects' communicative behaviours with a discrimination of the different postural clues (body and head orientation) available in our experimental conditions. This study suggests that capuchins can flexibly use a communicative gesture to adapt to the attentional state of their partner and provides evidence that acquired communicative gestures of monkeys might be used intentionally.

Sea lions' (Zalophus californianus) use of human pointing gestures as referential cues.

This experiment investigated the ability of four human-socialized sea lions to exploit human communicative gestures in three different object-choice tasks based on directional cues emitted by their caretakers. In Study 1, three of the tested subjects were able to generalize their choice of the pointed target to variations of the basic pointing gestures (i.e., cross-body point, elbow point, foot point, and gaze only), from the very first trials. Study 2 showed that the subjects could follow the pointing gestures geometrically and select the correct target among four possible targets, two on each side of the informant. In Study 3, we tested the robustness of their tendency to follow a pointing gesture by hiding targets behind barriers. One subject was able to follow pointing gestures towards targets not visible at the moment of their decision without any training, despite the presence of another visible and directly accessible one. Taken together, these results suggest that sea lions were able to use the referential property of the human pointing gesture, because they were able to rely on extrapolating precise linear vectors along different pointing body parts in order to identify a precise object rather than merely a general direction. These findings support previous arguments that some non-domesticated species might have as great an ability to respond appropriately to pointing gestures as domesticated dogs. The potential roles of human-socialization and specific features of wild sea lions ecology are discussed.

Extraction of structural regularities by baboons (Papio Papio): Adjacent and nonadjacent repetition patterns differ in learnability.

Several animal species can discriminate between different sequential patterns based on repetitions of items (e.g., ABB vs. ABA), and generalize their performance to sequences made of novel elements but following the same underlying structure. This achievement suggests that these species possess the ability to abstract the sequences structures beyond exemplars. Developmental studies in humans suggest however that adjacent repetition patterns (e.g., ABB) are easier to extract than patterns based on a nonadjacent (e.g., ABA) repetitions. This study addressed this effect of adjacency from a comparative perspective. Seventeen Guinea baboons (Papio papio) were tested with an adaptation of the serial response time task. Results show that baboons successfully learned and generalized both adjacent and nonadjacent repetition patterns after extensive exposure to each pattern in 2 successive experimental phases (Experiment 1). However, when these patterns were presented interleaved within the same experimental phase and at equal frequencies (Experiment 2), or presented successively as in Experiment 1 but with less exposure trials (Experiment 3), baboons showed evidence of learning of the adjacent repetition pattern only. Overall, these data suggest that baboons are more sensitive to adjacent than nonadjacent repetitions. We argue that a strategy based on sole detection of the presence/absence of an adjacent repetition is therefore likely to be adopted by the tested animals in pattern learning studies contrasting adjacent versus nonadjacent repetition patterns, and that future studies may need to avoid this contrast to prevent the use of this strategy. (PsycInfo Database Record (c) 2021 APA, all rights reserved).

Baboons (Papio papio) Process a Context-Free but Not a Context-Sensitive Grammar.

Language processing involves the ability to master supra-regular grammars, that go beyond the level of complexity of regular grammars. This ability has been hypothesized to be a uniquely human capacity. Our study probed baboons' capacity to learn two supra-regular grammars of different levels of complexity: a context-free grammar generating sequences following a mirror structure (e.g., AB | BA, ABC | CBA) and a context-sensitive grammar generating sequences following a repeat structure (e.g., AB | AB, ABC | ABC), the latter requiring greater computational power to be processed. Fourteen baboons were tested in a prediction task, requiring them to track a moving target on a touchscreen. In distinct experiments, sequences of target locations followed one of the above two grammars, with rare violations. Baboons showed slower response times when violations occurred in mirror sequences, but did not react to violations in repeat sequences, suggesting that they learned the context-free (mirror) but not the context-sensitive (repeat) grammar. By contrast, humans tested with the same task learned both grammars. These data suggest a difference in sensitivity in baboons between a context-free and a context-sensitive grammar.

Regularity Extraction Across Species: Associative Learning Mechanisms Shared by Human and Non-Human Primates.

Extracting the regularities of our environment is a core cognitive ability in human and non-human primates. Comparative studies may provide information of strong heuristic value to constrain the elaboration of computational models of regularity learning. This study illustrates this point by testing human and non-human primates (Guinea baboons, Papio papio) with the same experimental paradigm, using a novel online learning measure. For local co-occurrence regularities, we found similar patterns of regularity extraction in baboons and humans. However, only humans extracted the more global sequence structure. It is proposed that only the first result that is common to both species should be used to constrain models of regularity learning. The second result indicates that the extraction of global regularities cannot be accounted for by mere associative learning mechanisms and suggests that humans probably benefit from their language recoding abilities for extracting these regularities. We propose to use a comparative approach to address a series of remaining theoretical questions, which will contribute to the development of a general theory of regularity learning.

Non-adjacent Dependencies Processing in Human and Non-human Primates.

Human and non-human primates share the ability to extract adjacent dependencies and, under certain conditions, non-adjacent dependencies (i.e., predictive relationships between elements that are separated by one or several intervening elements in a sequence). In this study, we explore the online extraction dynamics of non-adjacent dependencies in humans and baboons using a serial reaction time task. Participants had to produce three-target sequences containing deterministic relationships between the first and last target locations. In Experiment 1, participants from the two species could extract these non-adjacent dependencies, but humans required less exposure than baboons. In Experiment 2, the data show for the first time in a non-human primate species the successful generalization of sequential non-adjacent dependencies over novel intervening items. These findings provide new evidence to further constrain current theories about the nature and the evolutionary origins of the learning mechanisms allowing the extraction of non-adjacent dependencies.

Corollary Discharge Failure in an Oculomotor Task Is Related to Delusional Ideation in Healthy Individuals.

Predicting the sensory consequences of saccadic eye movements likely plays a crucial role in planning sequences of saccades and in maintaining visual stability despite saccade-caused retinal displacements. Deficits in predictive activity, such as that afforded by a corollary discharge signal, have been reported in patients with schizophrenia, and may lead to the emergence of positive symptoms, in particular delusions of control and auditory hallucinations. We examined whether a measure of delusional thinking in the general, non-clinical population correlated with measures of predictive activity in two oculomotor tasks. The double-step task measured predictive activity in motor control, and the in-flight displacement task measured predictive activity in trans-saccadic visual perception. Forty-one healthy adults performed both tasks and completed a questionnaire to assess delusional thinking. The quantitative measure of predictive activity we obtained correlated with the tendency towards delusional ideation, but only for the motor task, and not the perceptual task: Individuals with higher levels of delusional thinking showed less self-movement information use in the motor task. Variation of the degree of self-generated movement knowledge as a function of the prevalence of delusional ideation in the normal population strongly supports the idea that corollary discharge deficits measured in schizophrenic patients in previous researches are not due to neuroleptic medication. We also propose that this difference in results between the perceptual and the motor tasks may point to a dissociation between corollary discharge for perception and corollary discharge for action.