Name: investigating motor skill learning processes with a robotic manipulandum
Uploaded: 2017-02-12T15:00:00
Description: Watch this Scientific Journal Video about Investigating Motor Skill Learning Processes with a Robotic Manipulandum at JoVE.com

This research was supported by the Swiss National Science Foundation, the Betty and David Koetser Foundation for Brain Research and the ETH Foundation.

The experiments presented here were approved by the Veterinary Office of the Canton of Zurich, Switzerland and were carried out according to national and institutional regulations.
1. Feeding Conditions
NOTE: All training sessions are performed under a scheduled feeding protocol.
<ol>
	<li>Feed the rats 50 g/kg of standard chow once per day, after training is completed. This amount of food is sufficient to prevent major weight loss (body weight is &#62;90% of free...

<ol>
	<li>Irvine, K. -. A., 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=A+novel+method+for+assessing+proximal+and+distal+forelimb+function+in+the+rat:+the+Irvine,+Beatties+and+Bresnahan+(IBB)+forelimb+scale.">A novel method for assessing proximal and distal forelimb function in the rat: the Irvine, Beatties and Bresnahan (IBB) forelimb scale.</a> JoVE. (46), (2010).</li><li>Ballermann, M., Metz, G. A., McKenna, J. E., Klassen, F., Whishaw, I. Q. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=The+pasta+matrix+reaching+task:+a+simple+test+for+measuring+skilled+reaching+distance,+direction,+and+dexterity+in+rats.">The pasta matrix reaching task: a simple test for measuring skilled reaching distance, direction, and dexterity in rats.</a> J Neurosci Meth. 106 (1), 39-45 (2001).</li><li>Kemble, E. D., Wimmer, S. C., Konkler, A. P. <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+varied+prior+manipulatory+or+consummatory+behaviours+on+nut+opening,+predation,+novel+foods+consumption,+nest+building,+and+food+tablet+grasping+in+rats.">Effects of varied prior manipulatory or consummatory behaviours on nut opening, predation, novel foods consumption, nest building, and food tablet grasping in rats.</a> Behav Proc. 8 (1), 33-44 (1983).</li><li>Buitrago, M. M., Ringer, T., Schulz, J. B., Dichgans, J., Luft, A. R. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=Characterization+of+motor+skill+and+instrumental+learning+time+scales+in+a+skilled+reaching+task+in+rat.">Characterization of motor skill and instrumental learning time scales in a skilled reaching task in rat.</a> Behav Brain Res. 155 (2), 249-256 (2004).</li><li>Whishaw, I. Q., Pellis, S. 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+structure+of+skilled+forelimb+reaching+in+the+rat:+A+proximally+driven+movement+with+a+single+distal+rotatory+component.">The structure of skilled forelimb reaching in the rat: A proximally driven movement with a single distal rotatory component.</a> Behav Brain Res. 41 (1), 49-59 (1990).</li><li>Hays, S. A., 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+isometric+pull+task:+a+novel+automated+method+for+quantifying+forelimb+force+generation+in+rats.">The isometric pull task: a novel automated method for quantifying forelimb force generation in rats.</a> J Neurosci Meth. 212 (2), 329-337 (2013).</li><li>Sharp, K. G., Duarte, J. E., Gebrekristos, B., Perez, S., Steward, O., Reinkensmeyer, D. J. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=Robotic+Rehabilitator+of+the+Rodent+Upper+Extremity:+A+System+and+Method+for+Assessing+and+Training+Forelimb+Force+Production+after+Neurological+Injury.">Robotic Rehabilitator of the Rodent Upper Extremity: A System and Method for Assessing and Training Forelimb Force Production after Neurological Injury.</a> J Neurotrauma. 33 (5), 460-467 (2016).</li><li>Hays, S. A., 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+bradykinesia+assessment+task:+an+automated+method+to+measure+forelimb+speed+in+rodents.">The bradykinesia assessment task: an automated method to measure forelimb speed in rodents.</a> J Neurosci Meth. 214 (1), 52-61 (2013).</li><li>Meyers, E., 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+supination+assessment+task:+an+automated+method+for+quantifying+forelimb+rotational+function+in+rats.">The supination assessment task: an automated method for quantifying forelimb rotational function in rats.</a> J Neurosci Meth. 266, 11-20 (2016).</li><li>Lambercy, O., 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=Sub-processes+of+motor+learning+revealed+by+a+robotic+manipulandum+for+rodents.">Sub-processes of motor learning revealed by a robotic manipulandum for rodents.</a> Behav Brain Res. 278, 569-576 (2015).</li><li>Vigaru, B. C., 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=A+robotic+platform+to+assess,+guide+and+perturb+rat+forelimb+movements.">A robotic platform to assess, guide and perturb rat forelimb movements.</a> IEEE Trans. Neural Syst. Rehabil. Eng. 21 (5), 796-805 (2013).</li><li>Klein, A., Sacrey, L. -. A. R., Whishaw, I. Q., Dunnett, S. B. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=The+use+of+rodent+skilled+reaching+as+a+translational+model+for+investigating+brain+damage+and+disease.">The use of rodent skilled reaching as a translational model for investigating brain damage and disease.</a> Neurosci Biobehav Rev. 36 (3), 1030-1042 (2012).</li><li>Gharbawie, O. A., Whishaw, I. Q. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=Parallel+stages+of+learning+and+recovery+of+skilled+reaching+after+motor+cortex+stroke:+&amp;#34;Oppositions&amp;#34;+organize+normal+and+compensatory+movements.">Parallel stages of learning and recovery of skilled reaching after motor cortex stroke: &amp;#34;Oppositions&amp;#34; organize normal and compensatory movements.</a> Behav Brain Res. 175 (2), 249-262 (2006).</li><li>Palm&#233;r, T., Tamt&#232;, M., Halje, P., Enqvist, O., Petersson, P. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=A+system+for+automated+tracking+of+motor+components+in+neurophysiological+research.">A system for automated tracking of motor components in neurophysiological research.</a> J Neurosci Meth. 205 (2), 334-344 (2012).</li><li>Alaverdashvili, M., Whishaw, I. Q. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=A+behavioral+method+for+identifying+recovery+and+compensation:+Hand+use+in+a+preclinical+stroke+model+using+the+single+pellet+reaching+task.">A behavioral method for identifying recovery and compensation: Hand use in a preclinical stroke model using the single pellet reaching task.</a> Neurosci Biobehav Rev. 37 (5), 950-967 (2013).</li><li>Alaverdashvili, M., Whishaw, I. Q. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=Compensation+aids+skilled+reaching+in+aging+and+in+recovery+from+forelimb+motor+cortex+stroke+in+the+rat.">Compensation aids skilled reaching in aging and in recovery from forelimb motor cortex stroke in the rat.</a> Neurosci. 167 (1), 21-30 (2010).</li><li>Molina-Luna, K., 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=Dopamine+in+motor+cortex+is+necessary+for+skill+learning+and+synaptic+plasticity.">Dopamine in motor cortex is necessary for skill learning and synaptic plasticity.</a> PloS one. 4 (9), (2009).</li><li>VandenBerg, P. M., Hogg, T. M., Kleim, J. A., Whishaw, I. Q. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=Long-Evans+rats+have+a+larger+cortical+topographic+representation+of+movement+than+Fischer-344+rats:+A+microstimulation+study+of+motor+cortex+in+na&#305;&#776;ve+and+skilled+reaching-trained+rats.">Long-Evans rats have a larger cortical topographic representation of movement than Fischer-344 rats: A microstimulation study of motor cortex in na&#305;&#776;ve and skilled reaching-trained rats.</a> Brain Res Bull. 59 (3), 197-203 (2002).</li><li>Whishaw, I. Q., Gorny, B., Foroud, A., Kleim, J. A. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=Long-Evans+and+Sprague-Dawley+rats+have+similar+skilled+reaching+success+and+limb+representations+in+motor+cortex+but+different+movements:+some+cautionary+insights+into+the+selection+of+rat+strains+for+neurobiological+motor+research.">Long-Evans and Sprague-Dawley rats have similar skilled reaching success and limb representations in motor cortex but different movements: some cautionary insights into the selection of rat strains for neurobiological motor research.</a> Behav Brain Res. 145 (1-2), 221-232 (2003).</li><li>Harms, K. J., Rioult-Pedotti, M. S., Carter, D. R., Dunaevsky, A. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=Transient+Spine+Expansion+and+Learning-Induced+Plasticity+in+Layer+1+Primary+Motor+Cortex.">Transient Spine Expansion and Learning-Induced Plasticity in Layer 1 Primary Motor Cortex.</a> J Neurosci. 28 (22), 5686-5690 (2008).</li><li>Metz, G. A., Whishaw, I. Q. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=Skilled+reaching+an+action+pattern:+stability+in+rat+(Rattus+norvegicus)+grasping+movements+as+a+function+of+changing+food+pellet+size.">Skilled reaching an action pattern: stability in rat (Rattus norvegicus) grasping movements as a function of changing food pellet size.</a> Behav Brain Res. 116 (2), 111-122 (2000).</li></ol>

Skilled reaching tasks are commonly used to study motor skill acquisition as well as impairment of motor function under pathological conditions6. Reliable and unambiguous analysis of reaching behavior is essential for the study of cellular mechanisms underlying motor skill acquisition, as well as neurophysiological processes involved in loss and subsequent recovery of function in animal models of neurological disease. The results presented here show how spatial and temporal aspects of the pulling ...

Motor tasks are widely used to assess behavioral and neural changes related to motor learning or to alterations in motor function in neurological or pharmacological animal models. Fine motor function can be difficult to quantify in rodents, however. Tasks requiring manual dexterity, such as manipulation of cereal1, pasta2, or sunflower seeds3 are sensitive and do not require extensive training of the animal. Their main drawback is that these tasks yield mostly qualitative results and can be difficult to score unambiguously.
Skilled reaching tasks, such as variations of the single pellet reaching task are more straightforward to quantify4,5. However, kinematic factors that underlie successful execution of these tasks can only be inferred to a limited extent and require labor-intensive frame-by-frame video analysis.
Robotic devices have gained popularity as means of quantifying aspects of forelimb function and motor skill. Several automated reaching tasks are available. The majority focus on a single aspect of a forelimb movement, such as pulling of a handle along a linear guide6,7, simple distal limb movements8, or pronation and supination of the paw9. While these devices show promise for the analysis of motor function in, they only reflect the complex motor actions executed during single pellet reaching to a limited extend.
Here, we demonstrate the use of a three-degree-of-freedom robotic device, ETH Pattus, developed for training and assessment of various motor tasks in rats10,11. It records planar and rotational movement of rat forelimb movements in reach, grasp, and pulling tasks carried out in the horizontal plane. Rats interact with the robot via a 6 mm-diameter spherical handle that can be reached through a window in the testing cage (width: 15 cm, length: 40 cm, height: 45 cm) and moved in the horizontal plane (pushing and pulling movements) and rotated (pronation-supination movements). Thus, it enables the rat to carry out movements that approximate those executed during conventional single pellet reaching tasks. The window is 10 mm wide and located 50 mm above the cage floor. The handle is located 55 mm above the floor. A sliding door blocks access to the handle between reaching trials and opens when the robot reaches its start position and closes after a trial is completed. After a correctly executed movement, rats receive a food reward on the opposite side of the testing cage.
The robot is controlled via software and records output from 3 rotary encoders at 1000 Hz, resulting in information about the position of the handle in the horizontal plane, as well as its rotation angle (for details, see reference11). The conditions required for successful task execution are defined in the software prior to each training session (e.g. minimum required pulling distance and maximum deviation from midline in a reach-and-pull task). An initial standardized reference position of the handle is recorded with a fixed holder at the start of each training session. This reference is used for all trials within a session, assuring a constant start position of the handle for each trial. Constant positioning of the handle relative to the cage window is assured by alignment of marks on the cage and robot (Figure 1).
Video recordings of the reaching movements are recorded using a small high speed camera (120 frames/s, 640 x 480 resolution). A small display in the camera&#39;s view shows the rat&#39;s identification number, training session, trial number and trial result (success or failed). These videos are used to verify recorded results and to assess the effects of reaching movements that precede the touching, pulling or rotation of the handle.
Here, we demonstrate the use of this robotic platform in variations of a reach-and-pull task. This task can be trained within a period of time that is comparable to other skilled reaching paradigms and yields reproducible results. We describe a typical training protocol, as well as some of the main output parameters. Moreover, we show how minor changes in the used training protocol can result in altered time courses of behavioral outcomes that may represent independent subprocesses within the motor skill learning process.

<table border="0" cellpadding="0" cellspacing="0" width="679">
	<tbody>
		<tr height="21">
			<td height="21" style="height:21px;width:247px;">ETH Pattus</td>
			<td style="width:105px;"></td>
			<td style="width:136px;"></td>
			<td style="width:191px;">ETH Pattus was made by the Rehabilitation Engineering Laboratory of Prof. Gassert at ETH Zurich.&#160;</td>
		</tr>
		<tr height="21">
			<td height="21" style="height:21px;width:247px;">Training cage&#160;</td>
			<td style="width:105px;"></td>
			<td style="width:136px;"></td>
			<td>The plexiglass training cage was made in-house.&#160;</td>
		</tr>
		<tr height="42">
			<td height="42" style="height:42px;width:247px;">Pellet dispenser</td>
			<td style="width:105px;">Campden Instruments</td>
			<td align="right" style="width:136px;">80209</td>
			<td></td>
		</tr>
		<tr height="21">
			<td height="21" style="height:21px;width:247px;">45-mg dustless precision pellets</td>
			<td style="width:105px;">Bio-Serv</td>
			<td style="width:136px;">F0021-J</td>
			<td></td>
		</tr>
		<tr height="21">
			<td height="21" style="height:21px;width:247px;">GoPro Hero 3+ Silver Edition&#160;</td>
			<td style="width:105px;">digitec.ch</td>
			<td align="right">284528</td>
			<td>Small highspeed camera&#160;</td>
		</tr>
		<tr height="42">
			<td height="42" style="height:42px;width:247px;">Small display</td>
			<td style="width:105px;">Adafruit Industries</td>
			<td style="width:136px;">#50, #661</td>
			<td>128x32 SPI Oled display controlled via an Arduino Uno microcontroller and Labview software</td>
		</tr>
		<tr height="42">
			<td height="42" style="height:42px;width:247px;">Labview 2012</td>
			<td style="width:105px;">National Instruments</td>
			<td style="width:136px;">776678-3513</td>
			<td>ETH Pattus is compatible with more recent Labview versions.&#160;</td>
		</tr>
		<tr height="42">
			<td height="42" style="height:42px;width:247px;">Matlab 2014b</td>
			<td style="width:105px;">The Mathworks</td>
			<td style="width:136px;">MLALL</td>
			<td></td>
		</tr>
	</tbody>
</table>

investigating motor skill learning processes with a robotic manipulandum

Skilled reaching tasks are commonly used in studies of motor skill learning and motor function under healthy and pathological conditions, but can be time-intensive and ambiguous to quantify beyond simple success rates. Here, we describe the training procedure for reach-and-pull tasks with ETH Pattus, a robotic platform for automated forelimb reaching training that records pulling and hand rotation movements in rats. Kinematic quantification of the performed pulling attempts reveals the presence of distinct temporal profiles of movement parameters such as pulling velocity, spatial variability of the pulling trajectory, deviation from midline, as well as pulling success. We show how minor adjustments in the training paradigm result in alterations in these parameters, revealing their relation to task difficulty, general motor function or skilled task execution. Combined with electrophysiological, pharmacological and optogenetic techniques, this paradigm can be used to explore the mechanisms underlying motor learning and memory formation, as well as loss and recovery of function (e.g. after stroke).

Here, we show 3 variations of a reach-and pull task using male Long-Evans rats (10-12 weeks old). In the free-pull (FP) group (N = 6), rats were trained to pull the robot&#39;s handle for a 22 day period without lateral restrictions. Animals in the straight-pull 1 (SP1) group (N = 12) were trained to pull the handle without deviating more than 2 mm from midline. These animals transitioned directly from reward-touch (step 2.3) to straight-pull training (step 2.5). For both FP and SP1 anima...

Watch this Scientific Journal Video about Investigating Motor Skill Learning Processes with a Robotic Manipulandum at JoVE.com

Investigating Motor Skill Learning Processes with a Robotic Manipulandum

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.

Skilled reaching tasks are commonly used in studies of motor skill learning and motor function under healthy and pathological conditions, but can be ...

Research

JoVE Journal

Behavior

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

Reaching for and retrieving objects require precise and coordinated motor movements in the forelimb. When mice are repeatedly trained to grasp and ...

Methods to Explore the Influence of Top-down Visual Processes on Motor Behavior

Kinesthetic awareness is important to successfully navigate the environment. When we interact with our daily surroundings, some aspects of movement are ...

Compensatory Limb Use and Behavioral Assessment of Motor Skill Learning Following Sensorimotor Cortex Injury in a Mouse Model of Ischemic Stroke

Mouse models have become increasingly popular in the field of behavioral neuroscience, and specifically in studies of experimental stroke. As models ...

Stimulating the Lip Motor Cortex with Transcranial Magnetic Stimulation

Transcranial magnetic stimulation (TMS) has proven to be a useful tool in investigating the role of the articulatory motor cortex in speech perception. ...

Functional Near Infrared Spectroscopy of the Sensory and Motor Brain Regions with Simultaneous Kinematic and EMG Monitoring During Motor Tasks

There are several advantages that functional near-infrared spectroscopy (fNIRS) presents in the study of the neural control of human movement. It is ...

Quantifying Learning in Young Infants: Tracking Leg Actions During a Discovery-learning Task

Task-specific actions emerge from spontaneous movement during infancy. It has been proposed that task-specific actions emerge through a discovery-learning ...

Event-related Potentials During Target-response Tasks to Study Cognitive Processes of Upper Limb Use in Children with Unilateral Cerebral Palsy

Unilateral Cerebral Palsy (CP) is a neurodevelopmental disorder that is a very common cause of disability in childhood. It is characterized by unilateral ...

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. ...

Using Virtual Reality to Transfer Motor Skill Knowledge from One Hand to Another

As far as acquiring motor skills is concerned, training by voluntary physical movement is superior to all other forms of training (e.g. training by ...

The "Motor" in Implicit Motor Sequence Learning: A Foot-stepping Serial Reaction Time Task

This protocol describes a modified serial reaction time (SRT) task used to study implicit motor sequence learning. Unlike the classic SRT task that ...