Fagot & Paleressompoulle1 have published an automated learning device (ALDM) aimed at testing individual cognitive abilities in semi-free ranging monkeys. The main goal of our protocol is to use a network of ALDM test units to study social cognition in non-human primates.
Fagot & Paleressompoulle1 and Fagot & Bonte2 have published an automated learning device (ALDM) for the study of cognitive abilities of monkeys maintained in semi-free ranging conditions. Data accumulated during the last five years have consistently demonstrated the efficiency of this protocol to investigate individual/physical cognition in monkeys, and have further shown that this procedure reduces stress level during animal testing3. This paper demonstrates that networks of ALDM can also be used to investigate different facets of social cognition and in-group expressed behaviors in monkeys, and describes three illustrative protocols developed for that purpose. The first study demonstrates how ethological assessments of social behavior and computerized assessments of cognitive performance could be integrated to investigate the effects of socially exhibited moods on the cognitive performance of individuals. The second study shows that batteries of ALDM running in parallel can provide unique information on the influence of the presence of others on task performance. Finally, the last study shows that networks of ALDM test units can also be used to study issues related to social transmission and cultural evolution. Combined together, these three studies demonstrate clearly that ALDM testing is a highly promising experimental tool for bridging the gap in the animal literature between research on individual cognition and research on social cognition.
Experimental laboratory investigations of primate cognition have almost systematically favored the test of isolated animals4, depending on the issue tackled. This classical laboratory procedure has demonstrated its efficiency, and most of our knowledge on issues such as perception, memory, reasoning and abstract conceptualization comes from the test of isolated subjects. Testing isolated individuals conveys many practical advantages; this approach facilitates complex experimental designs combined with highly rigorous measurements (e.g., msec timing) of the behavior that would be otherwise inaccessible. However, this procedure also has its limits, when it comes to the study of social influences on cognition in particular. Researchers are often forced to leave the sophisticated laboratory environment in favor of large enclosures or wild contexts when their study involves social interactions among individuals. This choice has a cost as it is much more difficult to control the experimental factors and to measure their effects with the same level of precision outside of the laboratory. Understanding how real social interactions influence cognition is one of the most difficult scientific challenges in both humans and nonhuman primates.
The present paper presents a new experimental protocol aimed at alleviating this general difficulty to investigate social cognition in laboratory based nonhuman primates. Fagot & Paleressompoulle1 and Fagot & Bonte2 have recently published an automated learning device (ALDM) for the assessment of cognitive abilities of monkeys raised in semi-free conditions. This method combines the operant conditioning techniques traditionally used in laboratories with a Radio Frequency Identification (RFID) technology. In practice, monkeys living in their social group have a free access from their outdoor enclosure to several ALDM test units. ADLMs consist of open test systems containing all of the necessary equipment traditionally available in laboratories, in particular a touch screen to display the stimulus and record the response and a food dispenser to deliver the reward. A RFID microchip reader captures the numeric identity of the participant when it enters an ALDM test unit, and the test program uses this information to present the research program assigned to this particular subject.
Evidence accumulated during the past 5 years has clearly revealed that (1) ALDM testing enhances the motivation of the participants1,2 and (2) favors complex learning5,6. ALDM testing also seems beneficial in terms of animal welfare, and reduces the stress level of the participant3, see also7. The ALDM testing procedure inspired the development of test devices by several research groups working with crested (Macaca nigra) and rhesus (Macaca mulatta) macaques7,8 and pigeons (Columba livia)9. The main goal of our paper is to demonstrate the potential contribution of ALDM testing for studies in the domain of social cognition. Three different uses of this protocol are described for that purpose. The ALDM test units have already been described in details in Fagot & Paleressompoulle1. They are illustrated in Figure 1 and described briefly below. ALDM test units are open access operant conditioning test systems equipped with a Radio Frequency Identification (RFID) system that reads the RFID microchip of the monkey, and therefore its identity, once it enters the test system. The stimuli are presented on a touch screen, and food rewards are delivered inside the test system after a correct response is given (choice of the correct stimulus) to these stimuli.
Ethics statement: This research was carried out in accordance with French standards and received approval from the national French ethics committee, the “Comité d’Ethique CE-14 pour l’Expérimentation Animale”. Procedures were also consistent with the guidelines of the Association for the Study of Animal Behaviour.
1. ALDM Test Unit Set-up
NOTE: Set up the ALDM test units as per Fagot & Paleressompoulle1.
Figure 1: Picture (A) and schematic view (B) of an ALDM unit. Each test unit has five main component elements. (A) touchscreen; (B) handport; (C) viewport; (D) food dispenser delivering food items inside the cage after a correct response; (E) computer; (F) door providing access from the enclosure. Please click here to view a larger version of this figure.
2. ALDM Network Set-up
Figure 2: Schematic representation of the ALDM network. Each ALDM unit receives and provides information from/to a unique controlling server. Please click here to view a larger version of this figure.
3. Illustration of the Use of the ALDM Network for the Study of Social Cognition
NOTE: The ALDM protocol has the unique advantage of having monkeys that can interact freely with computers, while being maintained in their social group. Below are presented 3 protocols illustrating the use of a network of ALDM test units to collect unprecedented information on baboons’ (Papio papio) social cognition.
Figure 3: Schematic illustration of Section 3.1. The spontaneous behaviors expressed in the enclosure are recorded in parallel with the cognitive performance on the ALDM tests.
Figure 4: Schematic illustration of Section 3.3. The first baboon (Generation 1) had to complete a set of 50 trials generated by the computer. The motor responses of this baboon were then used to create the stimuli for the second baboon (Generation 2) in the transmission chain. This procedure was repeated until the last baboon in the chain was tested. Please click here to view a larger version of this figure.
As shown in Figure 5, the response times following negatively valenced behaviors, such as threats, were significantly slower than those following neutral (e.g., object manipulation), and positively valenced social behaviors, such as grooming. This study demonstrates that social moods affect the performance during cognitive testing. Interested readers will find more detailed information about this study in Marzouki et al.10 In Figure 6, compared to isolation, the presence of others reduced response times (the response time decreases with the number of individuals present in the trailer), indicating a social facilitation effect of well-learned responses. More detailed about this research can be found in Huguet et al.11 Figure 7 indicates an increase in performance during transmission trials (blue squares) but not in a control (random) condition (yellow circles). More detailed information on this research can be found in Claidière et al.12
Figure 5: Illustrative results from Section 3.1. Mean response times (msec) in the visual search task immediately following social positive, negative or neutral events. Error bars represent the standard deviation (SD).
Figure 6: Illustrative results from Section 3.2. Social presence effect on the speed of well-learned responses. This figure shows the mean response times (msec) depending on the number of conspecifics present during each trial in the adjacent ALDM test units. Error bars represent the standard error (SE).
Figure 7: Illustrative results from Section 3.3. The success of baboons (average number of rewards for 50 trials) increased with the number of transmission events (generation) during transmission trials (blue squares) but not during random control trials (yellow circles). Error bars represent the SE.
Primatologists have always expressed a strong interest in social and non-social aspects of cognition. However the integration of these two levels of understanding has been difficult. Social testing is sometimes conducted in laboratories, but on a very restricted number of subjects13. A network of ALDM units offers 4 main advantages in that respect: (1) ALDM testing uses highly sophisticated (computerized) protocols and millisecond precision measurements of the cognitive processes; (2) ALDM testing is achieved within the natural social context of the studied animals; (3) ALDM testing can be proposed to large groups, as done in our studies; (4) ALDM testing takes advantage of the spontaneous occurrence of social interactions and do not constrain the individuals to particular social situations.
ALDM network therefore opens avenues for integrative and multidimensional analyses of cognition combining social and non-social factors.
This paper illustrates this integrative approach using three protocols but many other possibilities exist beside these key illustrations. For instance, preliminary (unpublished) evidence collected in our laboratory suggests that the monkeys using adjacent test units also have the strongest affiliative bonds within their social group. If this effect is confirmed, then the automaticity of ALDM testing will allow the collection of large amount of information on social dynamics that can facilitate longitudinal sociometric studies (e.g., based on measures of social distance) in non-human primates.
The limitations of ALDM testing remain unknown at this stage. For instance, it is still unknown to what extent the activity level of the subjects can be influenced by the social structure (e.g., sex ratio) of the group. Nevertheless, ALDM testing seems a highly promising tool to bridge the apparent gap between studies on individual cognition and those more focused on social cognition. Its use offers the opportunity to identify the social factors that may influence individual cognition, and to more precisely measure their effects. Furthermore, our previous research has shown that ALDM testing also promotes animal welfare: They are forms of behavioral enrichments that reduce stress levels (inferred from cortisol level and the number of abnormal stereotypies)3. Accordingly, ALDM testing seems highly beneficial for both scientists and animals, and should be more extensively used in the future in laboratories and zoos.
The authors have nothing to disclose.
This research was supported by the “Federation de Recherche 3C”, Aix-Marseille University and the EU Euprim-Net-II project (#RII3-026155). This work was supported by a public grant overseen by the French National Research Agency (ANR) as part of the programs LICORNES (ANR-12-CULT-0002) and ASCE (ANR-13-PDOC-0004). The staff of the Rousset-sur-Arc CNRS primate station is acknowledged for technical support.
Touch screen | model ET1939L from Elotouch; Berwyn, IL | ||
RFID microchip reader | model Petscan RT100 Version 5, Real Trace; Villebon sur Yvette, France | ||
Eprime software | Professional, V 2.0, Psychology Software Tools, Pittsburg, PA | ||
PC-Computer connected to a network | HP-Pavillon in our laboratory | ||
Food dispenser | Home made in our laboratory |