Name: Acquisition of a High-precision Skilled Forelimb Reaching Task in Rats (Video) | JoVE Journal
Uploaded: 2015-06-22T15:00:00.000+00:00
Duration: 8 min 59 s
Description: Learn a high-precision skilled forelimb reaching task in rats to study motor learning phases and behavioral adaptations. This method enables detailed analysis of within-session and between-session learning in neuroscience research.

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This work was funded by grants of the Swiss National Science Foundation (Grant 31003A-149315-1 to M.E.S. and Grant IZK0Z3-150809 to A.Z.), to A.Z. the Heidi Demetriades Foundation, to M.E.S. the European Research Council (&#8216;Nogorise&#8217;) and the Christopher and Dana Reeve Foundation (CDRF).

All experiments were performed in accordance with the guidelines of the Veterinary Office of the Canton Zurich, Switzerland.
1. Animal Handling and Habituation
<ol>
	<li>Animal Handling 
	Note: 5 days prior to the start of the experiment, perform step 1.1.1 daily.
	<ol>
		<li>For behavioral experiments, accustom the animals to the experimenter. Have daily handling sessions lasting 10-15 min per animal. Clean the box after each animal&#8217;s session.
		<ol>
			<li>Initially, place the experimenter&#8217;s hand into a cage allowing the animal to explore and smell to become familiarized with the experimenter.</li>
			<li>Next, gently lift the animal with the experimenter&#8217;s hand in a safe manner by grasping the rat&#8217;s body between the front- and hind paws allowing further familiarization.</li>
		</ol>
		</li>
		<li>Weigh each animal daily to obtain a baseline bodyweight before food deprivation.</li>
	</ol>
	</li>
	<li>Apparatus Habituation and Food Familiarization
	<ol>
		<li>Weigh each animal daily to obtain a baseline bodyweight before food deprivation.</li>
		<li>Start food depriving rats 3 days prior to the beginning of pre-training on a standard laboratory diet. Give rats 0.05 g of food per 1 g bodyweight per day (e.g., a rat weighing 200 g, start with 10 g of food). Ensure bodyweight to not decrease more than 10% per day by monitoring bodyweight daily.
		<ol>
			<li>If several animals are held in one cage, dominant rats may eat more than less dominant ones. In case the bodyweight of an animal decreases, feed the animal separately instead of group feeding. Give water ad libitum.</li>
		</ol>
		</li>
		<li>To acquaint the rat with the grasping apparatus, place the animal into the training box (Figure 1). Have sugar pellets placed in the training box in proximity to the slit opening to familiarize the animal with the food pellets. Perform this step 10-15 min daily for 3 days.</li>
	</ol>
	</li>
</ol>
2. Pre-training and Motor Skill Learning
<ol>
	<li>Pre-training
	<ol>
		<li>One day after familiarization, place the animal into the training box and place the pellet closely to the slit opening so it can be reached by the animal&#8217;s tongue. Exclude animals that retrieve pellets with their forelimb during pre-training 
		Note: At this stage, pellet retrieval with the tongue is crucial and usually the animal&#8217;s method of choice. Pellets should be in no case grasped with the forelimb until the first day of motor skill learning to allow adequate monitoring of the learned reaching task. Pellet retrieval with the forelimb during pre-training is an exclusion criterion and is in most cases not observed.</li>
		<li>Teach the rat to either run to the rear of the cage and return to the slit opening or step back and turn around its own axis in order to receive the next food pellet with the tongue. Allow time for the animal to explore the cage, run to the rear and return to the slit opening. If the animal does not correctly execute the task, use a forceps to gently tap at the end rear of the cage and catch the animal&#8217;s attention. Once the animal is at the rear, gently tap at the cage front to guide the animal to the slit opening. 
		Note: Once the animal reaches a defined standard value (e.g., 50 successful pellet retrievals with the tongue in less than 15 min), the animal qualifies for the motor skill learning stage. On day 1 and 2 of pre-training, learners can already be distinguished from non-learners. Non-learners can be excluded from the study at this step. This decreases the probability of having a high number of non-learners during the motor learning step (2.2).</li>
		<li>During pre-training, food deprive rats on a standard laboratory diet. Give water ad libitum. Monitor body weight daily throughout the study. Do not use same room to train male and female rats. Ensure a calm and noise-free environment for the animal.</li>
	</ol>
	</li>
	<li>Determination of Paw Preference and Motor Skill Learning
	<ol>
		<li>During the first session of motor skill learning, replace the slide in front of the window with a post. Place the sugar pellet about 1.5 cm away from the window on the post so that the animal cannot reach the pellet with its tongue but only retrieve it by a precise forelimb reaching and grasping movement.
		<ol>
			<li>To enforce pellet retrieval by the forelimb, use a forceps to gently bring the pellet close to the animal&#8217;s mouth and retract the pellet while the animal attempts consumption with the tongue. Carry out this task repetitively until the animal stretches out the forelimb and grasps a pellet.</li>
		</ol>
		</li>
		<li>Place the post central to the window opening. To determine paw preference, carefully observe the first 10 trials on training day 1. More than 70% of the reaching attempts (i.e., 7 out of 10) have to be executed with the same forelimb. If this is not achieved, continue with another round of 10 trials until the 70% threshold is reached.</li>
		<li>After paw preference determination, shift the post towards the preferred forelimb and align central to the border of the window opening. Preferred paw alignment means the post is shifted contrary to the respective paw to allow an optimal angle for reaching (Figure 1B, C).</li>
		<li>Classify a trial, defined as a new pellet presented to the animal, as successful (reach, grasp, retrieve and eat the pellet), drop (reach, grasp and lose pellet during retrieval) or fail (knock pellet off the post). Note down every trial in your sheet and analyse the data after the experiment.</li>
		<li>Perform one daily session consisting of a defined number of trials (e.g., 150) or a maximum time (e.g., 1 hr) for each animal.</li>
		<li>Investigate precision and fine-tuning of the movement using first attempt analysis. A first attempt is defined by grasping of the pellet in a single monolithic movement without disruption, hesitation or repetition of individual movement components. Carefully observe each grasp by the rat.
		<ol>
			<li>If the rat hesitates or retracts during a reach or attempts several trials to correctly grasp the pellet, note the respective trial as success but not first attempt. If the animal successfully grasps the pellet in a single monolithic reach, note down the respective trial as successful first attempt in a separate column in your sheet.</li>
		</ol>
		</li>
		<li>During motor skill learning, food deprive rats on a standard laboratory diet. Give water ad libitum. Monitor body weight daily throughout the study.</li>
	</ol>
	</li>
</ol>

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<li>Zemmar, A., et al. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/pubmed?term=((Neutralization+of+Nogo-A+enhances+synaptic+plasticity+in+the+rodent+motor+cortex+and+improves+motor+learning+in+vivo%5BTitle%5D)+AND+%22The+Journal+of+neuroscience+%3A+the+official+journal+of+the+Society+for+Neuroscience%22%5BJournal%5D)">Neutralization of Nogo-A enhances synaptic plasticity in the rodent motor cortex and improves motor learning in vivo.</a> The Journal of neuroscience : the official journal of the Society for Neuroscience. 34, 8685-8698 (2014).</li>
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The authors have nothing to disclose

The paradigm shown in this study is adapted from Buitrago et al.18 and differs from the classical single pellet reaching paradigm17 mainly in two aspects:
First, studying within-session improvement allows analysis of the learned task within a single day, which can provide a different level of information such as investigation of the fast learning component compared to the slow learning component represented by the average daily values (see Figures 3</stro...

Movement control is a core function of the central nervous system (CNS). Motricity is the main measurable output of CNS function and the main possibility for individuals to interact with the external world. Understanding the principles of motor function and the mechanisms that underlie the learning of a motor task is currently one of the big challenges in neuroscience. Morphological, physiological and molecular changes were found upon acquisition of a new motor task. For example, the shape and number of synapses change in response to skilled motor training1-5, and functional changes of the synaptic machinery were observed after motor learning. Synaptic responses were higher in the connections of the forelimb-representing region of the trained motor cortex compared to the untrained hemisphere of the same animal or to responses from untrained animals6,7. Electrophysiological observations also suggest that long-term potentiation (LTP) and long-term depression (LTD) like mechanisms take place during the learning of a new motor skill, and that the range of synaptic operation, which is defined between the limiting borders of LTP and LTD saturation, is modified8. Furthermore, it has been shown that activity markers and plasticity promoting molecules such as c-fos, GAP-43, or BDNF but also plasticity inhibiting molecules such as Nogo-A display regulatory roles for learning-related neuronal plasticity9-16.
These advances towards a better understanding of the mechanisms underlying motor learning could only be achieved with the use of behavioral paradigms that allow precise control of the acquisition of a new motor skill, e.g., skilled forelimb-reaching. Only a well-structured behavioral task allows to monitor and capture correlative changes that occur upon learning and execution of the respective task. Here we visually demonstrate a modified version of the skilled forelimb single-pellet reaching task in rats adapted from Buitrago et al.17 The presented paradigm allows the analysis of movement acquisition within a daily training session (within-session) representing the fast learning component and primary acquisition as well as skilled motor learning over several sessions (between-session) representing the slow learning component and maintenance of the learned task18. Importantly, this behavioral paradigm increases the degree of difficulty and complexity of the motor skill task due to two features: First, the rats are trained to turn around their axis after each grasp and thus to realign their body prior to the next pellet reach and renew the body orientation, preventing constant movement execution from the same angle. Second, pellets are retrieved from a vertical post placed in front of the cage. Due to the small diameter of the post, pellets can easily be kicked off requiring a precise grasp for successful retrieval and preventing simple pulling of the pellet towards the animal.
Such complex behavioral testing allows deeper insights into the mechanisms underlying motor learning. Compared to mice, rats are superior in their performance of complex behavioral tasks and thus better suited for complex paradigms as presented in this study. Considering the increasing genetic possibilities available for rats19,20, the combination of precise and well controlled behavioral testing methods with genetic manipulations, imaging and physiological techniques represents a powerful toolbox to better understand the neurobiological basis of motor learning and memory.

<table><tbody><tr><td>Training box</td><td></td><td></td><td>Self Made</td></tr><tr><td>Pedestal</td><td></td><td></td><td>Self Made</td></tr><tr><td>Sugar pellets</td><td>TSE Systems Intl. Group</td><td></td><td>45 mg dustless precision pellets</td></tr><tr><td>Sprague Dawley rats</td><td></td><td></td><td>5-6 week old males</td></tr><tr><td>Laptop computer</td><td>Hewlett Packard</td><td></td><td></td></tr><tr><td>Stop Watch</td><td></td><td></td><td></td></tr><tr><td>Forceps</td><td>Fine Science Tools (FST)</td><td></td><td></td></tr><tr><td>Excel</td><td>Microsoft</td><td></td><td></td></tr><tr><td>Prism</td><td>GraphPad</td><td></td><td></td></tr><tr><td>Weighing scale</td><td></td><td></td><td></td></tr><tr><td>Counter</td><td></td><td></td><td></td></tr></tbody></table>

acquisition of a high-precision skilled forelimb reaching task in rats

Acquisition of a High-precision Skilled Forelimb Reaching Task in Rats

Movements are the main measurable output of central nervous system function. Developing behavioral paradigms that allow detailed analysis of motor learning and execution is of critical importance in order to understand the principles and processes that underlie motor function. Here we present a paradigm to study movement acquisition within a daily session of training (within-session) representing the fast learning component and primary acquisition as well as skilled motor learning over several training sessions (between-session) representing the slow learning component and consolidation of the learned task. This behavioral paradigm increases the degree of difficulty and complexity of the motor skill task due to two features: First, the animal realigns its body prior to each pellet retrieval forcing renewed orientation and preventing movement execution from the same angle. Second, pellets are grasped from a vertical post that matches the diameter of the pellet and is placed in front of the cage. This requires a precise grasp for successful pellet retrieval and thus prevents simple pulling of the pellet towards the animal. In combination with novel genetics, imaging and electrophysiological technologies, this behavioral method will aid to understand the morphological, anatomical and molecular underpinnings of motor learning and memory.

Successful motor skill acquisition is only achieved through consistent practice. Despite careful consideration of all aspects, some rats fail to learn the task (Figure 2). These 'non-learners' either lack motivation resulting in few or absent attempts of pellet retrieval from the start of the experiment or generally lose interest in reaching for the pellets leading to continuously failed attempts. By contrast, some animals show aggressive and over-motivated behavior resulting in overhasty and rushed gras...

A paradigm is presented to analyze the acquisition of a high-precision skilled forelimb reaching task in rats.

Movements are the main measurable output of central nervous system function. Developing behavioral paradigms that allow detailed analysis of motor ...

The overall goal of this procedure is to study the acquisition of a complex four limb reaching task and the analysis of its two phases within session learning and between session learning. This is accomplished by first familiarizing the animal with the experimenter and the learning environment. The second step is to teach the rat to realign its body prior to each food pellet retrieval with the tongue.Next, the rat learns how to grasp with its four limbs for the sugar pellet placed on a pedestal. Once its preferred, forelimb is determined, the pedestal is shifted to optimize the angle of access for pellet grasping during the training period, each trial is scored as a success, a drop, or a failure. The main advantage of this technique or existing methods, like the classical single palate reaching task, is to increase the difficulty of motor learning, allowing the investigation of more complex foreign movements.Visual demonstration of this method is critical as the different steps are difficult to explain in a manuscript text, seeing, hearing, and reading the individual steps, allowing more complete way to explain the technique. To prepare the animals for the experiment, handle them daily for at least five days, proceeding the experiments such sessions should take 10 to 15 minutes per animal. Utilize this opportunity to weigh them.When initially handling a rat, just let the animals get used to your hand being in their cage. Then gently lift the animal in a safe manner. Weigh each animal to establish their baseline body weight prior to food deprivation.Three days before the pre-training begins during the habituation period, start the starvation protocol. Give the rats just 0.05 grams of standard diet per gram of body weight. Daily access to water should not be restricted.Make sure that each rat does not lose more than 10%of its body weight during the period of food restriction. If several animals are held in one cage, it will probably be necessary to feed them separately so the dominant animal does not eat all the food. To acquaint the rat with the grasping apparatus, put it into the training box for five days prior to the start of pre-training with daily sessions lasting 10 to 15 minutes.Also place several pellets into the training box to familiarize the animal with their smell and taste. Lastly, between exposure to each animal, be sure to clean the training box. Male and female rats must be trained in separate rooms.The training room must be calm and quiet. Preferably do not mix male and female rats in the same study. After the rats have been familiarized with the training box, start the pre-training.Return each rat to the box and place a sugar pellet on the slide in front of the slid opening so the animal can reach it with its tongue. Now teach the rat to either run to the rear of the cage and return to the slit opening for the next pellet, or to step back and turn around its own access. To get another pellet.Allow the rat to explore the cage during execution of this task. If the rat fails to do this properly, gently tap the rear of the cage with forceps to catch its attention. Once the rat goes to the rear of the cage, gently tap the front of the cage to attract its attention.Back to the slit opening. This step will take patience Pal. Retrieval with the tongue is crucial at this stage, and usually the animal's method of choice.An attempt of pal retrieval with the for during the pre-training period is D For an exclusion criteria Define having learned the task as when the rat can execute it a certain number of times within a timeframe, such as 50 tongue pellet, retrievals within 15 minutes, train each rat daily for up to an hour until the criteria are met. Non learner rats can usually be identified within a few days of pre-training. They should be excluded from the study during the pre-training.It is important to continue starving the rats. They should retain free access to water, and their weight should be monitored daily. For the task learning, replace the slide in front of the training box with a pedestal.Then place the pellet on the pedestal, which is 1.5 centimeters away from the window so that it cannot be reached by the tongue, but only with a forelimb. To teach the animal how to grasp the pellet, move the pellet close to the rat's mouth using forceps, and then retract it. When the rat sticks out its tongue and attempts to lick it, continue teasing the rat in this way until it stretches out.Its forelimb to grasp the pellet. During the first 10 reaching attempts, the pedestal is positioned in the middle of the slit opening to determine the paw preference. If seven or more of the first 10 trials are accomplished with the same forelimb that paw is considered as the preferred paw, if this threshold is not reached, continue looking through subsequent 10 trial blocks until a preference is shown.A preference must also be maintained between 10 trial blocks and generally is after determining preference. Shift the pedestal to the window border contrary to the preferred limb, thus giving the animal a better angle of access to the palate. With its preferred limb score each pellet presentation as a success, a drop or a failure.A drop includes a successful grasp followed by its loss. A success occurs when the rat successfully grasps the pellet and retrieves it to its mouth to finally eat the pellet. Perform one session per day.Use a trial number limit and a time limit to define the session duration. For example, end the session after either 150 pellet grasps or an hour, whichever comes first. Precision and fine tuning can be determined in the analysis of a rat's success on its first attempt to retrieve a pellet.Success on the first attempt occurs only when the rat makes a single monolithic movement. Without disruption, hesitation, or repetition of an individual movement component, always take note of these types of success. During the motor skill learning, it is important to continue starving the rats.As in pre-training, never hold back access to water and weigh each rat daily. While many rats learn the task, some fail, they may be unmotivated or lose interest. After several failures, they may be too rushed and aggressive to learn the task.There are also rats that show early success, but then lose their ability to improve or even drop in success. Success can be defined in two phases. An initial fast learning component representing primary acquisition is usually observed in the first training session.The second phase consists of skilled motor learning, which takes more time and represents consolidation of the learned task over several sessions. Rats take a varying number of days to accomplish this level of learning, resulting in averaged curves that are not too smooth. Another expression of successful motor learning can be seen in the fine tuning of the motor plan.In each training session, the fraction of pellets retrieved on a first attempt compared to all successes can measure this sort of motor learning. While attempting this procedure, it's important to stay calm, provide a comfortable and noise free environment during the sessions, and to food restrict the animals while monitoring their weights. This procedure can be combined with other methods, such as treatment with specific drugs, different imaging techniques, electrophysiology or genetic modifications.This multitude of experimental combinations offers a good basis for a better understanding of motor learning.

acquisition-of-a-high-precision-skilled-forelimb-reaching-task-in-rats

Research

JoVE Journal

Behavior

The skilled reaching scale divides the movement by a forelimb in a reach for food act into composite elements each of which are evaluated with a three-point scale. The rating scale is described for a normal rat and can be applied toward evaluating neurological motor disorders.

The Structure of Skilled Forelimb Reaching in the Rat: A Movement Rating Scale

The Vermicelli and Capellini Handling Tests of forepaw dexterity take advantage of the natural inclination of rodents to manipulate food items using skillful forepaw and digit movements. Animals are videotaped while handling short strands of uncooked dry pasta. Slow motion video playback allows for the quantification of forepaw adjustments.

The Vermicelli and Capellini Handling Tests: Simple quantitative measures of dexterous forepaw function in rats and mice

Persistent practice improves the precision of coordinated movements. Here we introduce a single-pellet reaching task, which is designed to assess the learning and memory of forelimb skill in...

Study Motor Skill Learning by Single-pellet Reaching Tasks in Mice

A paradigm is presented for training and analysis of an automated skilled reaching task in rats. Analysis of pulling attempts reveals distinct subprocesses of motor learning.

Investigating Motor Skill Learning Processes with a Robotic Manipulandum

This manuscript describes a semi-automated task that quantifies supination in rats. Rats reach, grasp, and supinate a spherical manipulandum. The rat is rewarded with a pellet if the turn angle exceeds a criterion set by the user. This task increases throughput, sensitivity to injury, and objectivity compared to traditional tasks.

The Knob Supination Task: A Semi-automated Method for Assessing Forelimb Function in Rats

Method to assess the impact of training on motor skills is a useful tool. Unfortunately, most behavioral assessments can be labor intensive and/or expensive.We describe here a robotic method of assessing prehension (reach-to-grasp) skill in mice.

Evaluating Skilled Prehension in Mice Using an Auto-Trainer

Rodent skilled reaching is commonly used to study dexterous skills, but requires significant time and effort to implement the task and analyze the behavior. We describe an automated version of skilled reaching with motion tracking and three-dimensional reconstruction of reach trajectories.

Automated Rat Single-Pellet Reaching with 3-Dimensional Reconstruction of Paw and Digit Trajectories

The present protocol describes how to use wireless optogenetics combined with high-speed videography in a single pellet reach-to-grasp task to characterize the neural circuits involved in the performance of skilled motor behavior in freely moving mice.

In Vivo Wireless Optogenetic Control of Skilled Motor Behavior

The current study describes a fine motor behavior test for examining motor deficits in rodent models, including the TgF344-AD rat, using machine learning.

A Fine Motor Task to Study Joint Kinematics in a Preclinical Model of Neurodegenerative Disease

We demonstrate how an objective measure can be employed in the widely employed rubber hand illusion paradigm. This measure is obtained by modifying the well-established crossmodal congruency task. This task allows the investigation of multisensory processes which are critical for modulations of body representations as in the rubber hand illusion.

The Crossmodal Congruency Task as a Means to Obtain an Objective Behavioral Measure in the Rubber Hand Illusion Paradigm

Learn a high-precision skilled forelimb reaching task in rats to study motor learning phases and behavioral adaptations. This method enables detailed analysis of within-session and between-session learning in neuroscience research.

Acquisition of a High-precision Skilled Forelimb Reaching Task in Rats

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