Name: assessment of social cognition in non-human primates using a network of computerized automated learning device (aldm) test systems
Uploaded: 2015-05-05T15:00:00
Duration: 8 min 42 s
Description: 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

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. 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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 border="0" cellpadding="0" cellspacing="0" width="806">
	<tbody>
		<tr height="106">
			<td height="106" style="height:106px;width:301px;">Touch screen</td>
			<td style="width:345px;"></td>
			<td style="width:80px;"></td>
			<td style="width:80px;">model ET1939L from Elotouch; Berwyn, IL</td>
		</tr>
		<tr height="169">
			<td height="169" style="height:169px;width:301px;">RFID microchip reader</td>
			<td style="width:345px;"></td>
			<td style="width:80px;"></td>
			<td style="width:80px;">model Petscan RT100 Version 5, Real Trace; Villebon sur Yvette, France</td>
		</tr>
		<tr height="148">
			<td height="148" style="height:148px;width:301px;">Eprime software</td>
			<td style="width:345px;"></td>
			<td style="width:80px;"></td>
			<td style="width:80px;">Professional, V 2.0, Psychology Software Tools, Pittsburg, PA</td>
		</tr>
		<tr height="22">
			<td height="22" style="height:22px;width:301px;">PC-Computer connected to a network</td>
			<td style="width:345px;">HP-Pavillon in our laboratory</td>
			<td></td>
			<td></td>
		</tr>
		<tr height="22">
			<td height="22" style="height:22px;width:301px;">Food dispenser</td>
			<td style="width:345px;">Home made in our laboratory&#160;</td>
			<td></td>
			<td></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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Modulating Cognition Using Transcranial Direct Current Stimulation of the Cerebellum

Numerous studies have emerged recently that demonstrate the possibility of modulating, and in some cases enhancing, cognitive processes by exciting brain regions involved in working memory and attention using transcranial electrical brain stimulation. Some researchers now believe the cerebellum supports cognition, possibly via a remote neuromodulatory effect on the prefrontal cortex. This paper describes a procedure for investigating a role for the cerebellum in cognition using transcranial direct current stimulation (tDCS), and a selection of information-processing tasks of varying task difficulty, which have previously been shown to involve working memory, attention and cerebellar functioning. One task is called the Paced Auditory Serial Addition Task (PASAT) and the other a novel variant of this task called the Paced Auditory Serial Subtraction Task (PASST). A verb generation task and its two controls (noun and verb reading) were also investigated. All five tasks were performed by three separate groups of participants, before and after the modulation of cortico-cerebellar connectivity using anodal, cathodal or sham tDCS over the right cerebellar cortex. The procedure demonstrates how performance (accuracy, verbal response latency and variability) could be selectively improved after cathodal stimulation, but only during tasks that the participants rated as difficult, and not easy. Performance was unchanged by anodal or sham stimulation. These findings demonstrate a role for the cerebellum in cognition, whereby activity in the left prefrontal cortex is likely dis-inhibited by cathodal tDCS over the right cerebellar cortex. Transcranial brain stimulation is growing in popularity in various labs and clinics. However, the after-effects of tDCS are inconsistent between individuals and not always polarity-specific, and may even be task- or load-specific, all of which requires further study. Future efforts might also be guided towards neuro-enhancement in cerebellar patients presenting with cognitive impairment once a better understanding of brain stimulation mechanisms has emerged.

Transcranial direct current stimulation (tDCS) over the cerebellum exerts a remote effect on the prefrontal cortex, which can modulate cognition and performance. This was demonstrated using two information-processing tasks of varying complexity, whereby only cathodal tDCS improved performance when the task was difficult, but not easy.

Numerous studies have emerged recently that demonstrate the possibility of modulating, and in some cases enhancing, cognitive processes by exciting brain ...

Experimental Assessment of Mouse Sociability Using an Automated Image Processing Approach

Mouse is the preferred model organism for testing drugs designed to increase sociability. We present a method to quantify mouse sociability in which the test mouse is placed in a standardized apparatus and relevant behaviors are assessed in three different sessions (called session I, II, and III).
The apparatus has three compartments (see Figure 1), the left and right compartments contain an inverted cup which can house a mouse (called &#34;stimulus mouse&#34;).
In session I, the test mouse is placed in the cage and its mobility is characterized by the number of transitions made between compartments. In session II, a stimulus mouse is placed under one of the inverted cups and the sociability of the test mouse is quantified by the amounts of time it spends near the cup containing the enclosed stimulus mouse vs. the empty inverted cup. In session III, the inverted cups are removed and both mice interact freely. The sociability of the test mouse in session III is quantified by the number of social approaches it makes toward the stimulus mouse and by the number of times it avoids a social approach by the stimulus mouse.
The automated evaluation of the movie detects the nose of the test mouse, which allows the determination of all described sociability measures in session I and II (in session III, approaches are identified automatically but classified manually). To find the nose, the image of an empty cage is digitally subtracted from each frame of the movie and the resulting image is binarized to identify the mouse pixels. The mouse tail is automatically removed and the two most distant points of the remaining mouse are determined; these are close to nose and base of tail. By analyzing the motion of the mouse and using continuity arguments, the nose is identified.
<img alt="Figure 1" src="/files/ftp_upload/52508/52508fig1.jpg" /> 
Figure 1. Assessment of Sociability During 3 sessions. Session I (top): Acclimation of test mouse to the cage. Session II (middle): Test mouse moving freely in the cage while the stimulus mouse is enclosed in an inverted cup. Session III (bottom): Both test mouse and stimulus mouse are allowed to move freely and interact with each other.

This protocol describes a method to quantify mouse sociability. Mice are videotaped as they move and interact in a special cage. Movie processing allows for the automated quantification of sociability with excellent accuracy and reliability.

Mouse is the preferred model organism for testing drugs designed to increase sociability. We present a method to quantify mouse sociability in which the ...

The Modified Hole Board - Measuring Behavior, Cognition and Social Interaction in Mice and Rats

This protocol describes the modified hole board (mHB), which combines features from a traditional hole board and open field and is designed to measure multiple dimensions of unconditioned behavior in small laboratory mammals (e.g., mice, rats, tree shrews and small primates). This paradigm is a valuable alternative for the use of a behavioral test battery, since a broad behavioral spectrum of an animal&#8217;s behavioral profile can be investigated in one single test.
The apparatus consists of a box, representing the &#8216;protected&#8217; area, separated from a group compartment. A board, on which small cylinders are staggered in three lines, is placed in the center of the box, representing the &#8216;unprotected&#8217; area of the set-up. The cognitive abilities of the animals can be measured by baiting some cylinders on the board and measuring the working and reference memory. Other unconditioned behavior, such as activity-related-, anxiety-related- and social behavior, can be observed using this paradigm. Behavioral flexibility and the ability to habituate to a novel environment can additionally be observed by subjecting the animals to multiple trials in the mHB, revealing insight into the animals&#8217; adaptive capacities.
Due to testing order effects in a behavioral test battery, na&#239;ve animals should be used for each individual experiment. By testing multiple behavioral dimensions in a single paradigm and thereby circumventing this issue, the number of experimental animals used is reduced. Furthermore, by avoiding social isolation during testing and without the need to food deprive the animals, the mHB represents a behavioral test system, inducing if any, very low amount of stress.

This protocol describes the modified hole board, which is a behavioral test set-up that comprises the characteristics of an open field and a traditional hole board. This set-up enables the differential analysis of unconditioned behavior of small laboratory mammals as well as the analysis of cognitive abilities.

This protocol describes the modified hole board (mHB), which combines features from a traditional hole board and open field and is designed to measure ...

The Double-H Maze: A Robust Behavioral Test for Learning and Memory in Rodents

Spatial cognition research in rodents typically employs the use of maze tasks, whose attributes vary from one maze to the next. These tasks vary by their behavioral flexibility and required memory duration, the number of goals and pathways, and also the overall task complexity. A confounding feature in many of these tasks is the lack of control over the strategy employed by the rodents to reach the goal, e.g., allocentric (declarative-like) or egocentric (procedural) based strategies. The double-H maze is a novel water-escape memory task that addresses this issue, by allowing the experimenter to direct the type of strategy learned during the training period. The double-H maze is a transparent device, which consists of a central alleyway with three arms protruding on both sides, along with an escape platform submerged at the extremity of one of these arms.
Rats can be trained using an allocentric strategy by alternating the start position in the maze in an unpredictable manner (see protocol 1; &#167;4.7), thus requiring them to learn the location of the platform based on the available allothetic cues. Alternatively, an egocentric learning strategy (protocol 2; &#167;4.8) can be employed by releasing the rats from the same position during each trial, until they learn the procedural pattern required to reach the goal. This task has been proven to allow for the formation of stable memory traces.
Memory can be probed following the training period in a misleading probe trial, in which the starting position for the rats alternates. Following an egocentric learning paradigm, rats typically resort to an allocentric-based strategy, but only when their initial view on the extra-maze cues differs markedly from their original position. This task is ideally suited to explore the effects of drugs/perturbations on allocentric/egocentric memory performance, as well as the interactions between these two memory systems.

The goal of this protocol is to investigate spatial cognition in rodents. The double-H water maze is a novel test, which is particularly useful to elucidate the different components of learning, consolidation and memory, as well as the interplay of memory systems.

Spatial cognition research in rodents typically employs the use of maze tasks, whose attributes vary from one maze to the next. These tasks vary by their ...

The Social Dimension of Stress: Experimental Manipulations of Social Support and Social Identity in the Trier Social Stress Test

In many situations humans are influenced by the behavior of other people and their relationships with them. For example, in stressful situations supportive behavior of other people as well as positive social relationships can act as powerful resources to cope with stress. In order to study the interplay between these variables, this protocol describes two effective experimental manipulations of social relationships and supportive behavior in the laboratory. In the present article, these two manipulations are implemented in the Trier Social Stress Test (TSST)&#8212;a standard stress induction paradigm in which participants are subjected to a simulated job interview. More precisely, we propose (a) a manipulation of the relationship between different protagonists in the TSST by making a shared social identity salient and (b) a manipulation of the behavior of the TSST-selection committee, which acts either supportively or unsupportively. These two experimental manipulations are designed in a modular fashion and can be applied independently of each other but can also be combined. Moreover, these two manipulations can also be integrated into other stress protocols and into other standardized social interactions such as trust games, negotiation tasks, or other group tasks.

Previous research on the social dimension of stress has focused on two important variables: social identity and social support. This protocol introduces an effective experimental manipulation of these two social variables and describes their implementation in a standard stress induction paradigm (Trier Social Stress Test).

In many situations humans are influenced by the behavior of other people and their relationships with them. For example, in stressful situations ...

Using a Split-belt Treadmill to Evaluate Generalization of Human Locomotor Adaptation

Understanding the mechanisms underlying locomotor learning helps researchers and clinicians optimize gait retraining as part of motor rehabilitation. However, studying human locomotor learning can be challenging. During infancy and childhood, the neuromuscular system is quite immature, and it is unlikely that locomotor learning during early stages of development is governed by the same mechanisms as in adulthood. By the time humans reach maturity, they are so proficient at walking that it is difficult to come up with a sufficiently novel task to study de novo locomotor learning. The split-belt treadmill, which has two belts that can drive each leg at a different speed, enables the study of both short- (i.e., immediate) and long-term (i.e., over minutes-days; a form of motor learning) gait modifications in response to a novel change in the walking environment. Individuals can easily be screened for previous exposure to the split-belt treadmill, thus ensuring that all experimental participants have no (or equivalent) prior experience. This paper describes a typical split-belt treadmill adaptation protocol that incorporates testing methods to quantify locomotor learning and generalization of this learning to other walking contexts. A discussion of important considerations for designing split-belt treadmill experiments follows, including factors like treadmill belt speeds, rest breaks, and distractors. Additionally, potential but understudied confounding variables (e.g., arm movements, prior experience) are considered in the discussion.

We describe a protocol for investigating human locomotor adaptation using the split-belt treadmill, which has two belts that can drive each leg at a different speed. We specifically focus on a paradigm designed to test the generalization of adapted locomotor patterns to different walking contexts (e.g., gait speeds, walking environments).

Understanding the mechanisms underlying locomotor learning helps researchers and clinicians optimize gait retraining as part of motor rehabilitation. ...

Large Volume, Behaviorally-relevant Illumination for Optogenetics in Non-human Primates

This protocol describes a large-volume illuminator, which was developed for optogenetic manipulations in the non-human primate brain. The illuminator is a modified plastic optical fiber with etched tip, such that the light emitting surface area is &#62; 100x that of a conventional fiber. In addition to describing the construction of the large-volume illuminator, this protocol details the quality-control calibration used to ensure even light distribution. Further, this protocol describes techniques for inserting and removing the large volume illuminator. Both superficial and deep structures may be illuminated. This large volume illuminator does not need to be physically coupled to an electrode, and because the illuminator is made of plastic, not glass, it will simply bend in circumstances when traditional optical fibers would shatter. Because this illuminator delivers light over behaviorally-relevant tissue volumes (&#8776; 10 mm3) with no greater penetration damage than a conventional optical fiber, it facilitates behavioral studies using optogenetics in non-human primates.

A protocol to build a tissue penetrating illuminator for delivering light over large volumes with minimal diameter is presented.

This protocol describes a large-volume illuminator, which was developed for optogenetic manipulations in the non-human primate brain. The illuminator is a ...

Assessment of Social Transmission of Food Preferences Behaviors

Olfactory recognition deficits are suggested to be able to serve as clinical marker to differentiate Alzheimer&#39;s disease (AD) subjects from healthy aging groups. For example, olfactory dysfunction in AD can present as impairment in olfactory recognition, emerging during early stages of the disease and worsening while the disease progresses. The social transmission of food preferences (STFP) task is based on a rudimentary form of communication between rodents concerning distant foods dependent on the transmission of olfactory cues. Healthy wild-type mice would prefer to eat a novel, flavored food that was previously cued by a conspecific, and this food preference would be hampered in transgenic AD mice, such as the APP/PS1 model. Indeed, a strong preference for the cued food in C57Bl6/J mice of 3 months of age was found, and this was reduced in 3 months old transgenic APP/PS1 mice. In summary, STFP task could be a powerful measure to be integrated in present subclinical detection assays of AD.

This paper presents a protocol for the investigation of social transmission of food preference in mice. The advantages and possible applications for this procedure, for instance, in detecting early changes in AD mouse models, are highlighted. To conclude, interpretation of the results in light of critical details are discussed.

Olfactory recognition deficits are suggested to be able to serve as clinical marker to differentiate Alzheimer&#39;s disease (AD) subjects from healthy ...

Computerized Adaptive Testing System of Functional Assessment of Stroke

The computerized adaptive testing system of the functional assessment of stroke (CAT-FAS) can simultaneously assess four functions (motor functions of the upper and lower extremities, postural control, and basic activities of daily living) with sufficient reliability and administrative efficiency. CAT, a modern measurement method, aims to provide a reliable estimate of the examinee's level of function rapidly. CAT administers only a few items whose item difficulties match an examinee's level of function and, thus, the administered items of CAT can provide sufficient information to reliably estimate the examinee's level of function in a short time. The CAT-FAS was developed through four steps: (1) determining the item bank, (2) determining the stopping rules, (3) validating the CAT-FAS, and (4) establishing a platform of online administration. The results of this study indicate that the CAT-FAS has sufficient administrative efficiency (average number of items = 8.5) and reliability (group-level Rasch reliability: 0.88 - 0.93; individual-level Rasch reliability: &#8805;70% of patients had Rasch reliability score &#8805;0.90) to simultaneously assess four functions in patients with stroke. In addition, because the CAT-FAS is a computer-based test, the CAT-FAS has three additional advantages: the automatic calculation of scores, the immediate storage of data, and the easy exporting of data. These advantages of the CAT-FAS will be beneficial to data management for clinicians and researchers.

Here, we present a protocol to develop the computerized adaptive testing system of the functional assessment of stroke (CAT-FAS). The CAT-FAS can simultaneously assess four functions (two motor functions [upper and lower extremities], postural control, and basic activities of daily living) with sufficient reliability and administrative efficiency.

The computerized adaptive testing system of the functional assessment of stroke (CAT-FAS) can simultaneously assess four functions (motor functions of the ...

Using the FishSim Animation Toolchain to Investigate Fish Behavior: A Case Study on Mate-Choice Copying In Sailfin Mollies

Over the last decade, employing computer animations for animal behavior research has increased due to its ability to non-invasively manipulate the appearance and behavior of visual stimuli, compared to manipulating live animals. Here, we present the FishSim Animation Toolchain, a software framework developed to provide researchers with an easy-to-use method for implementing 3D computer animations in behavioral experiments with fish. The toolchain offers templates to create virtual 3D stimuli of five different fish species. Stimuli are customizable in both appearance and size, based on photographs taken of live fish. Multiple stimuli can be animated by recording swimming paths in a virtual environment using a video game controller. To increase standardization of the simulated behavior, the prerecorded swimming path may be replayed with different stimuli. Multiple animations can later be organized into playlists and presented on monitors during experiments with live fish.
In a case study with sailfin mollies (Poecilia latipinna), we provide a protocol on how to conduct a mate-choice copying experiment with FishSim. We utilized this method to create and animate virtual males and virtual model females, and then presented these to live focal females in a binary choice experiment. Our results demonstrate that computer animation may be used to simulate virtual fish in a mate-choice copying experiment to investigate the role of female gravid spots as an indication of quality for a model female in mate-choice copying.
Applying this method is not limited to mate-choice copying experiments but can be used in various experimental designs. Still, its usability depends on the visual capabilities of the study species and first needs validation. Overall, computer animations offer a high degree of control and standardization in experiments and bear the potential to &#39;reduce&#39; and &#39;replace&#39; live stimulus animals as well as to &#39;refine&#39; experimental procedures.

Using the FishSim Animation Toolchain to Investigate Fish Behavior: A Case Study on Mate-Choice Copying In Sailfin Mollies

Using the novel FishSim Animation Toolchain, we present a protocol for non-invasive visual manipulation of public information in the context of mate-choice copying in sailfin mollies. FishSim Animation Toolchain provides an easy-to-use framework for the design, animation and presentation of computer-animated fish stimuli for behavioral experiments with live test fish.