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.

Ethics statement: This research was carried out in accordance with French standards and received approval from the national French ethics committee, the &#8220;Comit&#233; d&#8217;Ethique CE-14 pour l&#8217;Exp&#233;rimentation Animale&#8221;. 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 &#38; Paleressompoulle1.
<ol>
	<li>Create test chambers of dimension (0.7 x 0.7 x 0.8 m3) as described in1. Ensure that each test chamber has 2 lateral transparent sidewalls. Equip each test chamber with a sliding door that can be open or closed on the backside (see Figure 1). Open the back door of the ALDM unit to provide access to the test system from the enclosure.</li>
	<li>Fit the front panel of the test chamber with a (7.3 x 7 cm2) view port providing vision of a 19 in touch screen located in front of the unit, and 2 handports for manual interactions with the touch screen.</li>
	<li>Install an antenna connected to a microchip reader around each hand port as described in1. The antenna will capture the RFID identity of the subject.</li>
	<li>Install a 19 in capacitive touch screen in front of each test chamber. The touchscreen serves to present the stimuli and to record response related variables (accuracy and response time). Separate the viewports 25 cm from the screen.</li>
	<li>Connect a PC computer to each test unit that will serve to run the test program. 
	NOTE: On each trial, the test program determines the test regimen of the subjects (e.g., property of the display, stimulus duration, etc.) and associates the behavioral measures (e.g., response time, accuracy) to the monkey identified by the RFID technology.</li>
	<li>Connect a food dispenser to the PC computer via a parallel port, as described in1. This dispenser delivers grains of dry wheat inside the ALDM monkey area.</li>
	<li>Inject a RFID microchip in the forearm of each individual of the group as described in1. 
	NOTE: This procedure should be performed according to the veterinarian practices.</li>
</ol>
<img alt="Figure 1" src="/files/ftp_upload/52798/52798fig1highres.jpg" width="700" /> 
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. <a href="https://www.jove.com/files/ftp_upload/52798/52798fig1highres.jpg" target="_blank">Please click here to view a larger version of this figure.</a>
2. ALDM Network Set-up
<ol>
	<li>Install 10 ALDM units inside two 8 x 4 m2 trailers, with 5 ALDM units in each trailer as described in1. Connect each ALDM test unit to a unique controlling server accessible via an IP address (see Figure 2). Ensure that the ALDM unit can both download and upload information from/to the server.</li>
	<li>Write a computer testing program that downloads text files from the server once a monkey is identified by an ALDM test unit as per1. In the text file, provide indications on the current experimental status (number of trials already performed in the training or testing phase) of the monkey using the unit. Write the testing program such that it can use that information for presenting the training or test trial predefined by the experimental procedure.</li>
	<li>Insert the test program inline script such that it uploads and downloads data from the server. Ensure that the ALDM unit synchronizes the ALDM clock twice a day. 
	NOTE: With this procedure, the 10 ALDM units can provide indications on which monkey uses which unit, and when, and therefore provide information on the social dynamics in the use of the test systems.</li>
	<li>Write the testing program such that before each trial, the test program uploads information from the server on the current experimental status of the monkey. Once the trial is complete, the ALDM unit will update the subject&#8217;s text file on the server. 
	NOTE: Centralization of the subject&#8217;s related parameters on the controlling server guarantees that the participants will be tested in the predefined test order, independently of ALDM test units it decides to use.</li>
	<li>Store the following data as a text file after each trial: Date, Day time (HH:MM:SS format), Name of the current test program, Monkey name, Number assigned to the ALDM test unit (e.g., 1), Test level (e.g., training), Score (1 = correct behavioral response; 2 = incorrect response), Response time with msec precision.</li>
</ol>
<img alt="Figure 2" src="/files/ftp_upload/52798/52798fig2highres.jpg" width="700" /> 
Figure 2: Schematic representation of the ALDM network. Each ALDM unit receives and provides information from/to a unique controlling server. <a href="https://www.jove.com/files/ftp_upload/52798/52798fig2highres.jpg" target="_blank">Please click here to view a larger version of this figure.</a>
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&#8217; (Papio papio) social cognition.
<ol>
	<li>Computerized ALDM testing combining behavioral (ethological) observations: 
	NOTE: The main goal of this research is to assess the effects of the valence (positive vs. negative) of affective states on the animals&#8217; cognitive performance during computerized ALDM testing. The procedure is outlined in Figure 3 and full details on this research were published in Marzouki et al.10
	<ol>
		<li>Install a visual search task consisting of the selection of a target visual stimulus among several distractors on each computer.</li>
		<li>During eight days, observe and record manually which behavior each individual exhibits in the enclosure, and when, with a timer synchronized to the controlling server.</li>
		<li>Group the behaviors exhibited in the enclosure in three clusters corresponding to the emotionally positive social events (e.g., grooming), the emotionally negative social events (e.g., threat), and the emotionally nonsocial (neutral) events (e.g., object manipulation).</li>
		<li>Analyze the response times of the visual search task obtained within a 3 min time window following a behavioral observation in the enclosure. Synchronize the behavioral observations and computer data and analyze (see Figure 3).</li>
	</ol>
	</li>
</ol>
<img alt="Figure 3" src="/files/ftp_upload/52798/52798fig3.jpg" /> 
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.
<ol start="2">
	<li>Assessment of social influences during ALDM testing: 
	NOTE: This protocol is aimed at studying audience effects on cognitive performance recorded during computerized ALDM testing. Full details on this research were published in Huguet et al.11
	<ol>
		<li>On each ALDM test unit, install a task in which a circle is followed by a response on the right side of the screen or on the left side when a parallelogram is presented.</li>
		<li>Allow the monkey to use the 10 ALDM test systems as they want. Several monkeys can therefore use adjacent test systems. Record which individual uses which system. 
		NOTE: The baboons can see their conspecifics (when present) using the other test setups of the trailer, thanks to the transparent side walls of each unit.</li>
		<li>Make sure that the test program records the performance of each individual, as well as the social context of the trial (i.e., if the other ALDM test units are simultaneously used, and by whom).</li>
		<li>Analyze variations in response time depending on the social context.</li>
	</ol>
	</li>
	<li>Cultural evolution assessed via computerized transfer of information from individuals to individuals: 
	NOTE: This protocol was developed to study the evolution of information transmitted through a chain of participants. The procedure is outlined in Figure 4 and full details on this research were published in Claidi&#232;re et al.12
	<ol>
		<li>Train the participants to solve a simple memory task in which they first see four randomly chosen red squares in a four by four grid of otherwise white ones. After 400 msec change all the red squares to white, and ask the participant to touch the squares that were previously red.</li>
		<li>When the training is completed, use the behavioral response of one participant (the squares touched) to produce the stimuli for the next individual in the chain (see Figure 4). Except for the first individual in the chain for which the grids are randomly generated by the computer.</li>
		<li>Analyze the success at the task with the number of transmission events.</li>
	</ol>
	</li>
</ol>
<img alt="Figure 4" src="/files/ftp_upload/52798/52798fig4highres.jpg" width="600" /> 
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. <a href="https://www.jove.com/files/ftp_upload/52798/52798fig2highres.jpg" target="_blank">Please click here to view a larger version of this figure.</a>

<ol>
	<li>Fagot, J., Paleressompoulle, D. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=Automatic+testing+of+cognitive+performance+in+baboons+maintained+in+social+groups.">Automatic testing of cognitive performance in baboons maintained in social groups.</a> Behav Res Methods. 41 (2), 396-404 (2009).</li><li>Fagot, J., Bont&#233;, E. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=Automated+testing+of+cognitive+performance+in+monkeys:+Use+of+a+battery+of+computerized+test+systems+by+a+troop+of+semi-free+ranging+baboons.">Automated testing of cognitive performance in monkeys: Use of a battery of computerized test systems by a troop of semi-free ranging baboons.</a> Behav Res Methods. 42 (2), 507-516 (2010).</li><li>Fagot, J., Gullstrand, J., Kemp, C., Defilles, C., Mekaouche, M. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=Effects+of+freely+accessible+computerized+test+systems+on+the+spontaneous+behaviors+and+stress+level+of+Guinea+baboons+(Papio+papio).">Effects of freely accessible computerized test systems on the spontaneous behaviors and stress level of Guinea baboons (Papio papio).</a> Am J Primatol. 76 (1), 10-1002 (2014).</li><li>Dr&#233;a, C. M. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=Studying+primate+learning+in+group+contexts:+Tests+of+social+foraging,+response+to+novelty,+and+cooperative+problem+solving.">Studying primate learning in group contexts: Tests of social foraging, response to novelty, and cooperative problem solving.</a> Methods. 38 (3), 162-177 (2006).</li><li>Grainger, J., Dufau, S., Montant, M., Ziegler, J. C., Fagot, J. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=Orthographic+processing+in+baboons.">Orthographic processing in baboons.</a> Science. 336 (6078), 245-248 (2012).</li><li>Fagot, J., Thompson, R. K. R. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=Generalized+Relational+Matching+by+Guinea+Baboons+(Papio+papio)+in+two+by+two-item+analogy+problems.">Generalized Relational Matching by Guinea Baboons (Papio papio) in two by two-item analogy problems.</a> Psychol Sci. 22 (10), 1304-1309 (2011).</li><li>Whitehouse, J., Micheletta, J., Powell, L. E., Bordier, C., Waller, B. M. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=The+Impact+of+Cognitive+Testing+on+the+Welfare+of+Group+Housed+Primates.">The Impact of Cognitive Testing on the Welfare of Group Housed Primates.</a> PLoS ONE. 8 (11), e78308 (2013).</li><li>Gazes, P. R., Brown, E. K., Basile, B. M., Hampton, R. R. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=Automated+cognitive+testing+of+monkeys+in+social+groups+yields+results+comparable+to+individual+laboratory-based+testing.">Automated cognitive testing of monkeys in social groups yields results comparable to individual laboratory-based testing.</a> Anim Cogn. 16 (3), 445-458 (2012).</li><li>Huber, L., Heise, N., Zenan, C., Palmers, C. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=The+ALDB+box:+Automatic+testing+of+cognitive+performance+in+groups+of+aviary-housed+pigeons.">The ALDB box: Automatic testing of cognitive performance in groups of aviary-housed pigeons.</a> Behav Res Methods. Apr 16 [Epub ahead of print]. , (2014).</li><li>Marzouki, Y. B., Gullstrrand, J., Goujon, A., Fagot, J. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=Baboons&#8217;+response+speed+is+biased+by+their+moods.">Baboons&#8217; response speed is biased by their moods.</a> PLoS One. 9 (7), e102562 (2014).</li><li>Huguet, P., Barbet, I., Belletier, C., Monteil, J. M., Fagot, J. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=Cognitive+control+under+social+influence+in+baboons.">Cognitive control under social influence in baboons.</a> Journal of Experimental Psychology : General. , (2014).</li><li>Claidi&#233;re, N., Smith, K., Kirby, S., Fagot, J. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=Cultural+evolution+of+systematically+structured+behaviour+in+a+non-human+primate.">Cultural evolution of systematically structured behaviour in a non-human primate.</a> Proc R Soc Lond B. 281 (1797), (2014).</li><li>Subiaul, F., Cantlon, J. F., Holloway, R. L., Terrace, H. S. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=Cognitive+imitation+in+Rhesus+macaques.">Cognitive imitation in Rhesus macaques.</a> Science. 305 (5682), 407-410 (2004).</li></ol>

The authors declare that no competing interests exist.

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.

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 &#38; Paleressompoulle1 and Fagot &#38; 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 &#38; 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.

<table><tbody><tr><td>Touch screen</td><td></td><td></td><td>model ET1939L from Elotouch; Berwyn, IL</td></tr><tr><td>RFID microchip reader</td><td></td><td></td><td>model Petscan RT100 Version 5, Real Trace; Villebon sur Yvette, France</td></tr><tr><td>Eprime software</td><td></td><td></td><td>Professional, V 2.0, Psychology Software Tools, Pittsburg, PA</td></tr><tr><td>PC computer connected to a network</td><td></td><td></td><td>HP-Pavillon, programmed in our laboratory</td></tr><tr><td>Food dispenser</td><td></td><td></td><td>Home made in our laboratory</td></tr></tbody></table>

assessment of social cognition in non-human primates using a network of computerized automated learning device (aldm) test systems

Fagot &#38; Paleressompoulle1 and Fagot &#38; 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.

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 Claidi&#232;re et al.12
<img alt="Figure 5" src="/files/ftp_upload/52798/52798fig5.jpg" width="500" /> 
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).
<img alt="Figure 6" src="/files/ftp_upload/52798/52798fig6.jpg" width="500" /> 
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).
<img alt="Figure 7" src="/files/ftp_upload/52798/52798fig7highres.jpg" width="500" /> 
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.

Watch this Scientific Journal Video about Assessment of Social Cognition in Non-human Primates Using a Network of Computerized Automated Learning Device ALDM Test Systems at JoVE.com

Assessment of Social Cognition in Non-human Primates Using a Network of Computerized Automated Learning Device ALDM Test Systems

Fagot &#38; 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.

Assessment of Social Cognition in Non-human Primates Using a Network of Computerized Automated Learning Device (ALDM) Test Systems

Fagot &#38; Paleressompoulle1 and Fagot &#38; Bonte2 have published an automated learning device (ALDM) for the study of cognitive abilities of monkeys ...

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12.0K Views.  Aix-Marseille University.  Fagot & Paleressompoulle 1 hebben een geautomatiseerde leren apparaat (ALDM) gericht op het testen van individuele cognitieve vaardigheden in semi-loslopende apen gepubliceerd. Het belangrijkste doel van ons protocol is om een ​​netwerk van ALDM testunits gebruiken om sociale cognitie te bestuderen in niet-menselijke primaten. 

Video: Assessment of Social Cognition in Non-human Primates Using a Network of Computerized Automated Learning Device ALDM Test Systems

Assessment of Social Interaction Behaviors

Social interactions are a fundamental and adaptive component of the biology of numerous species. Social recognition is critical for the structure and stability of the networks and relationships that define societies. For animals, such as mice, recognition of conspecifics may be important for maintaining social hierarchy and for mate choice 1.
A variety of neuropsychiatric disorders are characterized by disruptions in social behavior and social recognition, including depression, autism spectrum disorders, bipolar disorders, obsessive-compulsive disorders, and schizophrenia. Studies of humans as well as animal models (e.g., Drosophila melanogaster, Caenorhabditis elegans, Mus musculus, Rattus norvegicus) have identified genes involved in the regulation of social behavior 2. To assess sociability in animal models, several behavioral tests have been developed (reviewed in 3). Integrative research using animal models and appropriate tests for social behavior may lead to the development of improved treatments for social psychopathologies.
The three-chamber paradigm test known as Crawley's sociability and preference for social novelty protocol has been successfully employed to study social affiliation and social memory in several inbred and mutant mouse lines (e.g. 4-7). The main principle of this test is based on the free choice by a subject mouse to spend time in any of three box's compartments during two experimental sessions, including indirect contact with one or two mice with which it is unfamiliar. To quantitate social tendencies of the experimental mouse, the main tasks are to measure a) the time spent with a novel conspecific and b) preference for a novel vs. a familiar conspecific. Thus, the experimental design of this test allows evaluation of two critical but distinguishable aspects of social behavior, such as social affiliation/motivation, as well as social memory and novelty. "Sociability" in this case is defined as propensity to spend time with another mouse, as compared to time spent alone in an identical but empty chamber 7. "Preference for social novelty" is defined as propensity to spend time with a previously unencountered mouse rather than with a familiar mouse 7. This test provides robust results, which then must be carefully analyzed, interpreted and supported/confirmed by alternative sociability tests. In addition to specific applications, Crawley's sociability test can be included as an important component of general behavioral screen of mutant mice.

Here we describe a detailed protocol for examination of sociability in mice by using Crawley's sociability and preference for social novelty test. We describe the advantages and possible applications for this procedure, including critical details important for correct interpretation of the results.

Social interactions are a fundamental and adaptive component of the biology of numerous species. Social recognition is critical for the structure and ...

Neuroscience

Behavioral Assessment of Manual Dexterity in Non-Human Primates

The corticospinal (CS) tract is the anatomical support of the exquisite motor ability to skillfully manipulate small objects, a prerogative mainly of primates1. In case of lesion affecting the CS projection system at its origin (lesion of motor cortical areas) or along its trajectory (cervical cord lesion), there is a dramatic loss of manual dexterity (hand paralysis), as seen in some tetraplegic or hemiplegic patients. Although there is some spontaneous functional recovery after such lesion, it remains very limited in the adult. Various therapeutic strategies are presently proposed (e.g. cell therapy, neutralization of inhibitory axonal growth molecules, application of growth factors, etc), which are mostly developed in rodents. However, before clinical application, it is often recommended to test the feasibility, efficacy, and security of the treatment in non-human primates. This is especially true when the goal is to restore manual dexterity after a lesion of the central nervous system, as the organization of the motor system of rodents is different from that of primates1,2. Macaque monkeys are illustrated here as a suitable behavioral model to quantify manual dexterity in primates, to reflect the deficits resulting from lesion of the motor cortex or cervical cord for instance, measure the extent of spontaneous functional recovery and, when a treatment is applied, evaluate how much it can enhance the functional recovery.
The behavioral assessment of manual dexterity is based on four distinct, complementary, reach and grasp manual tasks (use of precision grip to grasp pellets), requiring an initial training of adult macaque monkeys. The preparation of the animals is demonstrated, as well as the positioning with respect to the behavioral set-up. The performance of a typical monkey is illustrated for each task. The collection and analysis of relevant parameters reflecting precise hand manipulation, as well as the control of force, are explained and demonstrated with representative results. These data are placed then in a broader context, showing how the behavioral data can be exploited to investigate the impact of a spinal cord lesion or of a lesion of the motor cortex and to what extent a treatment may enhance the spontaneous functional recovery, by comparing different groups of monkeys (treated versus sham treated for instance). Advantages and limitations of the behavioral tests are discussed. The present behavioral approach is in line with previous reports emphasizing the pertinence of the non-human primate model in the context of nervous system diseases2,3.

As manual dexterity is a prerogative mainly of primates, behavioral tasks have been developed in macaque monkeys. Four reach and grasp prehension tasks, measuring hand manipulation ability and force, allow to establish functional recovery after a lesion of the central nervous system and to test the effect of a treatment.

The corticospinal (CS) tract is the anatomical support of the exquisite motor ability to skillfully manipulate small objects, a prerogative mainly of ...

A Fully Automated and Highly Versatile System for Testing Multi-cognitive Functions and Recording Neuronal Activities in Rodents

We have developed a fully automated system for operant behavior testing and neuronal activity recording by which multiple cognitive brain functions can be investigated in a single task sequence. The unique feature of this system is a custom-made, acoustically transparent chamber that eliminates many of the issues associated with auditory cue control in most commercially available chambers. The ease with which operant devices can be added or replaced makes this system quite versatile, allowing for the implementation of a variety of auditory, visual, and olfactory behavioral tasks. Automation of the system allows fine temporal (10 ms) control and precise time-stamping of each event in a predesigned behavioral sequence. When combined with a multi-channel electrophysiology recording system, multiple cognitive brain functions, such as motivation, attention, decision-making, patience, and rewards, can be examined sequentially or independently.

In this report, we present a fully automated and highly versatile system capable of simultaneously testing multi-cognitive behaviors and recording neuronal activities for rodents.

We have developed a fully automated system for operant behavior testing and neuronal activity recording by which multiple cognitive brain functions can be ...

Testing for Metacognitive Responding Using an Odor-based Delayed Match-to-Sample Test in Rats

Metamemory involves the cognitive ability to assess the strength of one&#39;s memories. To explore the possibility of metamemory in non-human animals, numerous behavioral tasks have been created, many of which utilize an option to decline memory tests. To assess metamemory in rats, we utilized this decline-test option paradigm by adapting previous visual delayed-match-to-sample tests (DMTS)1,2 developed for primate species to an odor-based test suitable for rodents. First,&#160;rats are given a sample to remember by digging in a cup of scented sand. After a delay, the rat is presented with four distinctly scented cups, one of which contains the identical scent experienced during the sample; if this matching cup is selected, then the rat obtains a preferred, larger reward. Selection of any of the other three non-matching sand-filled scented cups results in no reward. Retention intervals are individually titrated such that subjects perform between 40 and 70% correct, therefore ensuring rats sometimes remember and sometimes forget the sample. Here, the operational definition of metamemory is the ability to distinguish between the presence and absence of memory through behavioral responding. Towards this end, on two-thirds of trials, a decline option is presented in addition to the four choice cups (choice trials). If the decline-test option- an unscented colored sand cup, is selected, the subject receives a smaller less-preferred reward and avoids the memory test. On the remaining third of trials, the decline-test option is not available (forced trials), causing subjects to guess the correct cup when the sample is forgotten. On choice tests, subjects that know when they remember should select the decline option when memory is weak rather than take the test and choose incorrectly. Therefore, significantly higher performance on chosen tests as compared to forced memory tests is indicative of the adaptive use of the decline-test response and metacognitive responding.

This protocol describes a method for investigating the possibility of metamemory, or memory awareness, in rodents. The odor-based delayed-matching-to-sample paradigm is a novel, ecologically-relevant behavioral test useful for determining the extent to which rodents can adaptively respond based on cognitively monitoring the strength of their memory states.

Metamemory involves the cognitive ability to assess the strength of one&#39;s memories. To explore the possibility of metamemory in non-human animals, ...

Automated, Long-term Behavioral Assay for Cognitive Functions in Multiple Genetic Models of Alzheimer's Disease, Using IntelliCage

Multiple factors&#8212;such as aging and genes&#8212;are frequently associated with cognitive decline. Genetically modified mouse models of cognitive decline, such as Alzheimer&#39;s disease (AD), have become a promising tool to elucidate the underlying mechanisms and promote the therapeutic advances. An important step is the validation and characterization of expected behavioral abnormality in the models, in the case of AD, cognitive decline. The long-term behavioral investigations of laboratory animals to study the effect of aging demand substantial efforts from researchers. The IntelliCage system is a high-throughput and cost-effective test battery for mice that eliminates the need for daily human handling. Here, we describe how the system is utilized in the long-term phenotyping of a genetic Alzheimer&#39;s disease model, specifically focusing on the cognitive functions. The experiment employs repeated battery of tests that assess spatial learning and executive functions. This cost-effective age-dependent phenotyping allows us to identify the transient and/or permanent effects of genes on various cognitive aspects.

This paper describes a protocol for cognitive assessments for genetic models of the Alzheimer&#39;s disease using the IntelliCage system, which is a high throughput automated behavioral monitoring system with operant conditioning.

Multiple factors&#8212;such as aging and genes&#8212;are frequently associated with cognitive decline. Genetically modified mouse models of cognitive ...

Noninvasive, In-pen Approach Test for Laboratory-housed Pigs

Traumatic brain injury (TBI) incidences have increased in both civilian and military populations, and many researchers are adopting a porcine model for TBI. Unlike rodent models for TBI, there are few behavioral tests that have been standardized. A larger animal requires more invasive handling in test areas than rodents, which potentially adds stress and variation to the animals&#39; responses. Here, the human approach test (HAT) is described, which was developed to be performed in front of laboratory pigs&#39; home pen. It is noninvasive, but flexible enough that it allows for differences in housing set-ups.
During the HAT, three behavioral ethograms were developed and then a formula was applied to create an approach index (AI). Results indicate that the HAT and its index, AI, are sensitive enough to detect mild and temporary alterations in pigs&#39; behavior after a mild TBI (mTBI). In addition, although specific behavior outcomes are housing-dependent, the use of an AI reduces variation and allows for consistent measurements across laboratories. This test is reliable and valid; HAT can be used across many laboratories and for various types of porcine models of injury, sickness, and distress. This test was developed for an optimized manual timestamping method such that the observer consistently spends no more than 9 min on each sample.

This protocol describes a new behavioral test&#8212;the human approach test in the pigs&#39; home pen&#8212;to detect functional deficits in laboratory pigs after subconcussive traumatic brain injury.

Traumatic brain injury (TBI) incidences have increased in both civilian and military populations, and many researchers are adopting a porcine model for ...

A System for Tracking the Dynamics of Social Preference Behavior in Small Rodents

Exploring the neurobiological mechanisms of social behavior requires behavioral tests that can be applied to animal models in an unbiased and observer-independent manner. Since the beginning of the millennium, the three-chamber test has been widely used as a standard paradigm to evaluate sociability (social preference) and social novelty preference in small rodents. However, this test suffers from multiple limitations, including its dependence on spatial navigation and negligence of behavioral dynamics. Presented and validated here is a novel experimental system that offers an alternative to the three-chamber test, while also solving some of its caveats. The system requires a simple and affordable experimental apparatus and publicly available open-source analysis system, which automatically measures and analyzes multiple behavioral parameters at individual and population levels. It allows detailed analysis of the behavioral dynamics of small rodents during any social discrimination test. We demonstrate the efficiency of the system in analyzing the dynamics of social behavior during the social preference and social novelty preference tests as performed by adult male mice and rats. Moreover, we validate the ability of the system to reveal modified dynamics of social behavior in rodents following manipulations such as whisker trimming. Thus, the system allows for rigorous investigation of social behavior and dynamics in small rodent models and supports more accurate comparisons between strains, conditions, and treatments.

Described here is a novel automated experimental system that offers an alternative to the three-chamber test and also solves several caveats. This system supplies multiple behavioral parameters that enable rigorous analysis of small rodent behavioral dynamics during the social preference and social novelty preference tests.

Exploring the neurobiological mechanisms of social behavior requires behavioral tests that can be applied to animal models in an unbiased and ...

Assessment of Mouse Judgment Bias through an Olfactory Digging Task

Judgment biases (JB) are differences in the way that individuals in positive and negative affective/emotional states interpret ambiguous information. This phenomenon has long been observed in humans, with individuals in positive states responding to ambiguity 'optimistically' and those in negative states instead showing 'pessimism'. Researchers aiming to assess animal affect have taken advantage of these differential responses, developing tasks to assess judgment bias as an indicator of affective state. These tasks are becoming increasingly popular across diverse species and fields of research. However, for laboratory mice, the most widely used vertebrates in research and a species heavily relied upon to model affective disorders, only one JB task has been successfully validated as sensitive to changes in affective state. Here, we provide a detailed description of this novel murine JB task, and evidence of its sensitivity to mouse affect. Though refinements are still necessary, assessment of mouse JB opens the door for answering both practical questions regarding mouse welfare, and fundamental questions about the impact of affective state in translational research.

This article provides a detailed description of a novel mouse judgment bias protocol. Evidence of this olfactory digging task's sensitivity to affective state is also demonstrated and its utility across diverse research fields is discussed.

Judgment biases (JB) are differences in the way that individuals in positive and negative affective/emotional states interpret ambiguous information. This ...

Behavioral Assays for Autism Spectrum Disorder in Mouse Models

Strategies for Assessing Autistic-Like Behaviors in Mice

Autism spectrum disorder (ASD) is a neurobiologically complex condition with a heterogeneous genetic etiology. Clinically, ASD is diagnosed by social communication impairments and restrictive or repetitive behaviors, such as hand flapping or lining up objects. These behavioral patterns can be reliably observed in mouse models with ASD-linked genetic mutations, making them highly useful tools for studying the underlying cellular and molecular mechanisms in ASD. Understanding how genetic changes affect the neurobiology and behaviors observed in ASD will facilitate the development of novel targeted therapeutic compounds to ameliorate core behavioral impairments. Our lab has employed several protocols encompassing well-described training and testing procedures that reflect a wide range of behavioral deficits related to ASD. Here, we detail two assays to study the core features of ASD in mouse models: self-grooming (a measure of repetitive behavior) and the three-chamber social interaction test (a measure of social interaction approach and preference for social novelty).

Rodent models are valuable tools for studying core behaviors related to autism spectrum disorder (ASD). In this article, we expound on two behavioral tests for modeling the core features of ASD in mice: self-grooming, which assesses repetitive behavior, and the three-chamber social interaction test, which documents social impairments.

Autism spectrum disorder (ASD) is a neurobiologically complex condition with a heterogeneous genetic etiology. Clinically, ASD is diagnosed by social ...

Assessment and Communication for People with Disorders of Consciousness

In this experiment, we demonstrate a suite of hybrid Brain-Computer Interface (BCI)-based paradigms that are designed for two applications: assessing the level of consciousness of people unable to provide motor response and, in a second stage, establishing a communication channel for these people that enables them to answer questions with either &#39;yes&#39; or &#39;no&#39;. The suite of paradigms is designed to test basic responses in the first step and to continue to more comprehensive tasks if the first tests are successful. The latter tasks require more cognitive functions, but they could provide communication, which is not possible with the basic tests. All assessment tests produce accuracy plots that show whether the algorithms were able to detect the patient&#39;s brain&#39;s response to the given tasks. If the accuracy level is beyond the significance level, we assume that the subject understood the task and was able to follow the sequence of commands presented via earphones to the subject. The tasks require users to concentrate on certain stimuli or to imagine moving either the left or right hand. All tasks are designed around the assumption that the user is unable to use the visual modality, and thus, all stimuli presented to the user (including instructions, cues, and feedback) are auditory or tactile.

With this experiment, one might be able to detect consciousness in people with disorders of consciousness. Furthermore, the approach can create a simple communication channel that enables people to give simple YES/NO answers to questions.

In this experiment, we demonstrate a suite of hybrid Brain-Computer Interface (BCI)-based paradigms that are designed for two applications: assessing the ...

Assessment of Social Cognition in Non-human Primates Using a Network of Computerized Automated Learning Device (ALDM) Test Systems

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