The authors are most grateful to Thomas Wacker for his technical support. We further thank Dr. Mirjam Roth for her kind support.

The handling of the rats and the experimental procedures were conducted in accordance with European, national, and institutional guidelines for animal care.
1. Acclimatization and Habituation
NOTE: If rats were not transported, the acclimatization and habituation time can be reduced. For noninvasive identification, color the tail with skin-friendly marker.
<ol>
	<li>Week 1: Acclimatization 
	NOTE: Two sessions should be performed during the f...

<ol>
	<li>Balcombe, J. P., Barnard, N. D., Sandusky, C. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=Laboratory+routines+cause+animal+stress.">Laboratory routines cause animal stress.</a> Contemporary Topics in Laboratory Animal Science. 43 (6), 42-51 (2004).</li><li>Sharp, J., Zammit, T., Azar, T., Lawson, D. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=Stress-like+responses+to+common+procedures+in+individually+and+group-housed+female+rats.">Stress-like responses to common procedures in individually and group-housed female rats.</a> Contemporary Topics in Laboratory Animal Science. 42 (1), 9-18 (2003).</li><li>Sharp, J. L., Zammit, T. G., Lawson, D. 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Merkblatt Nr. 160.</a> Heimtiere: Ratten. , (2014).</li><li>Cloutier, S., Panksepp, J., Newberry, R. C. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=Playful+handling+by+caretakers+reduces+fear+of+humans+in+the+laboratory+rat.">Playful handling by caretakers reduces fear of humans in the laboratory rat.</a> Applied Animal Behaviour Science. 140 (3-4), 161-171 (2012).</li><li>Bassett, L., Buchanan-Smith, H. M., McKinley, J., Smith, T. 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S., Ohl, F. <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+transportation+on+physiological+and+behavioral+parameters+in+Wistar+rats:+implications+for+acclimatization+periods.">The impact of transportation on physiological and behavioral parameters in Wistar rats: implications for acclimatization periods.</a> ILAR journal / National Research Council, Institute of Laboratory Animal Resources. 53 (1), 82-98 (2012).</li><li>Sotocina, S. G., et al. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=The+Rat+Grimace+Scale:+A+Partially+Automated+Method+for+Quantifying+Pain+in+the+Laboratory+Rat+via+Facial+Expressions.">The Rat Grimace Scale: A Partially Automated Method for Quantifying Pain in the Laboratory Rat via Facial Expressions.</a> Molecular Pain. 7, (2011).</li></ol>

The protocol described above is a useful extended application of our previously described clicker training protocol for laboratory mice10. The implementation requires only minutes per day over a total of seven weeks, including acclimatization, habituation and clicker training. For feasibility, this protocol was limited to week days with sessions of approximately ten minutes per pair of rats. The protocol can appear to be time-consuming to establish in large rat colonies, but if the animals are des...

Routine procedures can cause stress in laboratory animals1,2,3,4. It has been shown that cage changing does increase cardiovascular parameters and general activity in rats4,5,6. Such stress responses can at least be partially due to the physical disturbance and handling associated with cage changing procedures rather than the new unfamiliar environment2,4. Of particular importance is the negative effect of stress on the well-being of the regarded animal7. Further, stress induces changes in behavior and in other body parameters, including the autonomic nervous system, the neuroendocrine system and the immune system. Therefore, stress is often referred to as a possible source of unexpected deviations across animal experiments and should be avoided as much as possible in high-quality animal research7,8. One way to reduce stress in laboratory animals is by training. Training animals can generally be a very helpful tool for laboratory animal management and is, in fact, demanded by EU Directive 2010/63/EU9. Training can serve as a form of enrichment and helps to prepare animals for experiments; thus, training contributes to sustaining and enhancing well-being in laboratory settings10,11,12. A possible training method is positive reinforcement training (PRT). PRT is a form of operant conditioning where a reward (e.g., a food reward), is linked with a desired behavior13. This form of training is already commonly used in laboratory settings for nonhuman primates in order to reduce stress and to enhance well-being and has gained popularity in various other animal species10,13,14,15,16. Training of voluntary movement is also frequently used for refining animal husbandry management17,18,19. PRT is not only a helpful tool for cooperation when working with animals; it likewise is generally beneficial for the animals&#39; well-being, regardless of whether the trained behavior is directly used20. The positive reinforcement training protocol described here aims to avoid any form of stress during routinely performed cage changes by giving the rat the opportunity to voluntarily participate in the procedure.
In addition to the possible stress for the animals, working processes in animal facilities always provide pitfalls for the maintenance of hygiene status, especially as the direct contact between laboratory animals and animal caretakers bears the risk of hygiene contamination. In animal facilities specializing in rodents, the transfer of the animals from dirty into clean cages provides a regular and high workload. This procedure usually includes direct contact between animals and humans and thus represents a hygienic risk factor due to the possible transfer of pathogens settled on the human skin21. Aside from transfer from other animal vectors, pathogenic and nonpathogenic organisms intrude animal facilities most frequently via humans22,23. As reduced health is associated with reduced well-being, even subclinical infections can be a cause for nonreproducible experimental results, and this should clearly be avoided24,25. On this account, training animals to voluntary change cages further enables the conduction of the cage change after the training with hardly any direct contact between animal and animal caretaker, thereby reducing a potential hygienic risk while performing experimental procedures.
Our protocol for training rats to voluntarily change cages can be a helpful tool for laboratory rat management, as it links the training as a form of cognitive enrichment with performance of routine work. Accordingly, our protocol is an animal-friendly procedure that helps to increase the well-being of rats in laboratory animal facilities. As the cage change after the training phase can be performed with hardly any direct contact between animal and animal caretaker, it might additionally help to maintain hygiene at a high level and therefore further improve animal research.

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	<tbody>
		<tr height="20">
			<td height="20" style="height:20px;width:224px;">Target Stick with Clicker</td>
			<td style="width:111px;">Trixie</td>
			<td style="width:104px;">2282</td>
			<td style="width:280px;"></td>
		</tr>
		<tr height="20">
			<td height="20" style="height:20px;">Metal Pipe (Alu Flexrohr nw 100)</td>
			<td>Rotheigner</td>
			<td></td>
			<td>available in construction marktes</td>
		</tr>
		<tr height="20">
			<td height="20" style="height:20px;">White Chocolate/ white chocolate cream</td>
			<td></td>
			<td></td>
			<td>Company doesn&#39;t matter, preferable organic quality</td>
		</tr>
		<tr height="21">
			<td height="21" style="height:21px;">Prism Version 6.0 for Mac</td>
			<td>GraphPad Software</td>
			<td></td>
			<td></td>
		</tr>
	</tbody>
</table>

using clicker training and social observation to teach rats to voluntarily change cages

Cage cleaning is a routinely performed husbandry procedure and is known to induce stress in laboratory rats. As stress can have a negative impact on well-being and can affect the comparability and reproducibility of research results, the amount of stress experienced by laboratory animals should be minimized and avoided when possible. Further, the direct contact between the rat and animal caretaker during the cage change bears hygiene risks and therefore possibly negatively impacts the well-being of the rats and the quality of the research. 
Our protocol aims to improve the routinely performed cage changing procedure. For this reason, we present a feasible protocol that enables rats to learn via clicker training and observation to voluntarily change to a clean cage. This training helps to reduce stress caused by the physical disturbance and handling associated with the cage changes and concurrently enables a reduction in direct contact between animal and animal caretaker after the training phase is completed.
The implementation of clicker training to rats is fast and easy. Rats are generally interested in the training and efficiently learn the desired behavior, which entails changing cages through a pipe. Even without training, the rats learn to perform the desired behavior by observation, as 80% of the observational learning group successfully changed cages when tested. The training further helps to establish a relationship of trust between trainer and animal. As hygiene and well-being are both very important in animal experiments, this protocol might also help to improve high-quality research.

The training was conducted on a cohort of ten female Lister hooded (LD) rats. Ten untrained but gently handled female LD rats served as a control group. Gentle handling means that the rats were only lifted by their body and not lifted at the base of the tail. To evaluate the learning by observation, we added one further group of 10 female LD rats, which were not trained but were cage-mates of the trained rats and were able to observe the training. All rats completed the acclimatization an...

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Using Clicker Training and Social Observation to Teach Rats to Voluntarily Change Cages

This protocol introduces a method of cage change for rats via clicker training. Rats learn the desired behavior not only by direct training but also by observational learning. The implementation of this fast and easy protocol might help to improve well-being and hygiene in rodent facilities.

Cage cleaning is a routinely performed husbandry procedure and is known to induce stress in laboratory rats. As stress can have a negative impact on ...

This method can help to answer key questions in the emerging field of environment strategies for laboratory rodents, such as the stress reduction in routine husbandry procedures. The main advantage of this technique is that it can help to improve the routine process of cage-changing and in this way helps to improve the well-being of laboratory rats. Generally, individuals new to the method might struggle because the timing of the rewarding and the overall handling of the rats are critically important.First, bring the home cage to the training area, which should be a quiet place with limited distractions. Ensure that all required materials, such as the reward, the clicker, the target stick, a timer, the metal tube, a clean cage, and any other specific training materials are on hand. Critically observe the rats for any sign of discomfort throughout the procedure.Next, remove all items from the home cage. Only the trained rat and the observer rat and the bedding material should remain in the cage. Place a short tunnel in the home cage, preferably one made from a material that the rat is familiar with.Wait until the rat sits in the tunnel and then offer the rat the reward. As soon as the rat shows interest, and is about to start nibbling on the reward, click, and then let the rat feed on the reward. To ensure that the pairing of the two reinforcers is successful, repeat clicking, and then rewarding for 15 seconds.If the rat is not feeding under the circumstances of the training situation, the habituation phase must be extended or adjusted. If the rat did not participate, check for signs of a connection between the primary and the secondary reinforcer by administering the click without the reward. Signs of a connection include the rat sniffing for the reward, looking around for the reward, or lifting to its forelimbs to look for the reward.If this occurs, move on with the next part, otherwise, repeat training day one. For the next phase of training, place a short tunnel of the same material as the tunnel to be used to link the two cages. Start the timer and immediately begin with the first 30 seconds of training.The first time the rat shows interest in the tunnel, present the reward at the end of the tunnel. As soon as the rat enters the tunnel, click and then let the rat eat the reward. Take away the food reward and wait until the rat shows interest in the tunnel once more.Click as soon as the rat enters the tunnel and present the reward at the end of the tunnel. After 30 seconds of training, remove the tunnel for a 15-second break. Repeat the 30 seconds of training with the subsequent 15-second break for four minutes.If the rat shows the desired behavior more than four times a minute, stop clicking and just reward with the primary reinforcer. Start the timer and immediately begin with the first 30 seconds of training by placing the globe of the target stick near the rat. As soon as the rat shows interest in the globe, click and reward the rat.Repeat this several times. Add a break every 15 seconds and then go on with the training. If the rat shows interest in the globe more than four times a minute, the next behavior to reinforce is touching the globe with the nose.If the rat repeats that behavior for more than four times a minute, stop clicking and just reward with the primary reinforcer. Here, only the passing the tunnel towards the clean cage is reinforced. Build the connection between the home cage and a new clean cage by a tunnel by inserting a longer version of the tunnel already familiar to the rat.On day one, perform no training and just let the rats inspect the tunnel. There is a good chance that they will pass through the tunnel on their own. On day two, give the rat two minutes to transfer through the tunnel on its own from the dirty to the clean side.If the rat does not move through the tunnel, start the first 30-second training session by clicking and rewarding the rat as soon as it shows interest in the tunnel. Next, click and reward the rat's entrance into the tunnel and go on to click and reward if the rat goes deeper into the tunnel. Continue in a similar manner until the rat runs through the whole tunnel.As soon as the rat starts peeking from the end of the tunnel into the clean cage, present the globe of the target stick, click, and reward for touching the globe. Lastly, guide the rat to leave the tunnel. Present the globe in front of the tunnel and click and reward the rat as soon as it steps into the new cage and touches the globe.Put one hand under the belly or around the chest and support the hind legs of the rat to lift it out of the clean cage and place it back into the dirty cage. Then present the globe of the target stick in the center of the clean cage. Click and reward as the rat runs through the tunnel and touches the target stick.If the rat repeats the behavior for more than four times a minute, stop clicking and just reward with the primary reinforcer. 10 female Lister Hooded rats were trained to change cage via a metal pipe by clicker training. The training was evaluated in three categories.No participation, explorative behavior, and aimed behavior. All rats acquired the trained behavior after five days of training. After four weeks of observation, cage mates of trained rats were evaluated for voluntary cage-changing behavior.Overall, 80%of the observational learning group changed cages via the metal pipe. After four weeks of training, all rats were restrained and vocalizations, defecation, and urination were recorded and summed to calculate a fear-related behavior score for each rat. The untrained group showed an increased fear-related behavior score, compared to that of the trained and observational learning groups.While attempting this procedure, it's important to remember to observe the rats for any signs of discomfort and that all interactions must be in an animal-friendly way. Following this procedure, experiments in other scientific fields like behaviorism, neuroscience, or immunology can be performed with the benefit of happy, unstressed animals.

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JoVE Journal

Behavior

9.9K vistas.  Johannes Gutenberg-University Mainz. Este método puede ayudar a responder preguntas clave en el campo emergente de las estrategias ambientales para roedores de laboratorio, como la reducción del estrés en los procedimientos de cría rutinarios. La principal ventaja de esta técnica es que puede ayudar a mejorar el proceso rutinario de cambio de jaula y de esta manera ayuda a mejorar el bienestar de las ratas de laboratorio. Generalmente, individuos nuevos en el método podrían tener problemas porque el momento de la recompen...