The Vermicelli Handling Test: A simple quantitative measure of dexterous forepaw function in rats

Loss of function in the hands occurs with many brain disorders, but there are few measures of skillful forepaw use in rats available to model these impairments that are both sensitive and simple to administer. Whishaw and Coles previously described the dexterous manner in which rats manipulate food items with their paws, including thin pieces of pasta [Whishaw IQ, Coles BL. Varieties of paw and digit movement during spontaneous food handling in rats: postures, bimanual coordination, preferences, and the effect of forelimb cortex lesions. Behav Brain Res 1996;77:135-48]. We set out to develop a measure of this food handling behavior that would be quantitative, easy to administer, sensitive to the effects of damage to sensory and motor systems of the CNS and useful for identifying the side of lateralized impairments. When rats handle 7 cm lengths of vermicelli, they manipulate the pasta by repeatedly adjusting the forepaw hold on the pasta piece. As operationally defined, these adjustments can be easily identified and counted by an experimenter without specialized equipment. After unilateral sensorimotor cortex (SMC) lesions, transient middle cerebral artery occlusion (MCAO) and striatal dopamine depleting (6-hydroxydopamine, 6-OHDA) lesions in adult rats, there were enduring reductions in adjustments made with the contralateral forepaw. Additional pasta handling characteristics distinguished between the lesion types. MCAO and 6-OHDA lesions increased the frequency of several identified atypical handling patterns. Severe dopamine depletion increased eating time and adjustments made with the ipsilateral forepaw. However, contralateral forepaw adjustment number most sensitively detected enduring impairments across lesion types. Because of its ease of administration and sensitivity to lateralized impairments in skilled forepaw use, this measure may be useful in rat models of upper extremity impairment.

[1]  Jeff Biernaskie,et al.  Enriched Rehabilitative Training Promotes Improved Forelimb Motor Function and Enhanced Dendritic Growth after Focal Ischemic Injury , 2001, The Journal of Neuroscience.

[2]  S. Dunnett,et al.  The “staircase test”: a measure of independent forelimb reaching and grasping abilities in rats , 1991, Journal of Neuroscience Methods.

[3]  D. Corbett,et al.  An analysis of four different methods of producing focal cerebral ischemia with endothelin-1 in the rat , 2006, Experimental Neurology.

[4]  A. Castro,et al.  Motor performance in rats. The effects of pyramidal tract section. , 1972, Brain research.

[5]  D. R. McGiboney,et al.  Reeducation of handedness in the rat following cerebral injuries. , 1951, Journal of comparative and physiological psychology.

[6]  R. Ventura-Martínez,et al.  The sunflower seed test: a simple procedure to evaluate forelimb motor dysfunction after brain ischemia , 2006 .

[7]  Ian Q. Whishaw,et al.  The structure of skilled forelimb reaching in the rat: A proximally driven movement with a single distal rotatory component , 1990, Behavioural Brain Research.

[8]  G. M. Peterson Mechanisms of handedness in the rat , 1934 .

[9]  B. Kolb,et al.  A comparison of different models of stroke on behaviour and brain morphology , 2003, The European journal of neuroscience.

[10]  T. Jones,et al.  Unilateral ischemic sensorimotor cortical damage in female rats: forelimb behavioral effects and dendritic structural plasticity in the contralateral homotopic cortex , 2004, Experimental Neurology.

[11]  T. Jones,et al.  The behavioral and dendritic growth effects of focal sensorimotor cortical damage depend on the method of lesion induction , 2002, Behavioural Brain Research.

[12]  J. Kleim,et al.  Principles of experience-dependent neural plasticity: implications for rehabilitation after brain damage. , 2008, Journal of speech, language, and hearing research : JSLHR.

[13]  O. Witte,et al.  Motor improvements after focal cortical ischemia in adult rats are mediated by compensatory mechanisms , 2005, Behavioural Brain Research.

[14]  G. Schuierer,et al.  External carotid artery territory ischemia impairs outcome in the endovascular filament model of middle cerebral artery occlusion in rats. , 2003, Stroke.

[15]  Karim Nader,et al.  Functional Organization of Adult Motor Cortex Is Dependent upon Continued Protein Synthesis , 2003, Neuron.

[16]  S. Wise,et al.  The motor cortex of the rat: Cytoarchitecture and microstimulation mapping , 1982, The Journal of comparative neurology.

[17]  F. Colbourne,et al.  Constraint-Induced Movement Therapy and Rehabilitation Exercises Lessen Motor Deficits and Volume of Brain Injury After Striatal Hemorrhagic Stroke in Rats , 2003, Stroke.

[18]  S. Pellis,et al.  Impairments and compensation in mouth and limb use in free feeding after unilateral dopamine depletions in a rat analog of human Parkinson's disease , 1997, Behavioural Brain Research.

[19]  B. Kolb,et al.  Neonatal motor cortex lesions in the rat: absence of sparing of motor behaviors and impaired spatial learning concurrent with abnormal cerebral morphogenesis. , 1983, Behavioral neuroscience.

[20]  J. Larson,et al.  Effects of unilateral and bilateral training in a reaching task on dendritic branching of neurons in the rat motor-sensory forelimb cortex. , 1985, Behavioral and neural biology.

[21]  G. Schneider,et al.  Motor performance following unilateral pyramidal tract lesions in the hamster , 1975, Brain Research.

[22]  S. Pellis,et al.  Evidence for rodent-common and species-typical limb and digit use in eating, derived from a comparative analysis of ten rodent species , 1998, Behavioural Brain Research.

[23]  Ian Q Whishaw,et al.  The pasta matrix reaching task: a simple test for measuring skilled reaching distance, direction, and dexterity in rats , 2001, Journal of Neuroscience Methods.

[24]  Ian Q. Whishaw,et al.  Animal models of neurological deficits: how relevant is the rat? , 2002, Nature Reviews Neuroscience.

[25]  V. Bracha,et al.  The reaching reaction in the rat: A part of the digging pattern? , 1990, Behavioural Brain Research.

[26]  T. Jones,et al.  Motor Skill Training, but not Voluntary Exercise, Improves Skilled Reaching After Unilateral Ischemic Lesions of the Sensorimotor Cortex in Rats , 2008, Neurorehabilitation and neural repair.

[27]  I. Whishaw,et al.  On the origin of skilled forelimb movements , 2000, Trends in Neurosciences.

[28]  I. Whishaw Lateralization and reaching skill related: Results and implications from a large sample of Long-Evans rats , 1992, Behavioural Brain Research.

[29]  I. Whishaw,et al.  Varieties of paw and digit movement during spontaneous food handling in rats: Postures, bimanual coordination, preferences, and the effect of forelimb cortex lesions , 1996, Behavioural Brain Research.

[30]  M. Tuszynski,et al.  Lesions of the Basal Forebrain Cholinergic System Impair Task Acquisition and Abolish Cortical Plasticity Associated with Motor Skill Learning , 2003, Neuron.

[31]  T. Jones,et al.  Maladaptive effects of learning with the less-affected forelimb after focal cortical infarcts in rats , 2008, Experimental Neurology.

[32]  T. Jones,et al.  Behavioral and neuroplastic effects of focal endothelin-1 induced sensorimotor cortex lesions , 2004, Neuroscience.

[33]  Ian Q. Whishaw,et al.  Skilled forelimb movements in prey catching and in reaching by rats (Rattus norvegicus) and opossums (Monodelphis domestica): relations to anatomical differences in motor systems , 1996, Behavioural Brain Research.

[34]  I. Whishaw,et al.  The contributions of motor cortex, nigrostriatal dopamine and caudate-putamen to skilled forelimb use in the rat. , 1986, Brain : a journal of neurology.

[35]  I. Whishaw,et al.  An analysis of feeding and sensorimotor abilities of rats after decortication. , 1981, Journal of comparative and physiological psychology.

[36]  S. Butcher,et al.  Characterisation of an experimental model of stroke produced by intracerebral microinjection of endothelin-1 adjacent to the rat middle cerebral artery , 1995, Journal of Neuroscience Methods.

[37]  John D. Salamone,et al.  Ventrolateral striatal dopamine depletions impair feeding and food handling in rats , 1993, Pharmacology Biochemistry and Behavior.

[38]  Theresa A. Jones,et al.  Epidural cortical stimulation enhances motor function after sensorimotor cortical infarcts in rats , 2006, Experimental Neurology.

[39]  S. Pellis,et al.  Spontaneous forelimb grasping in free feeding by rats: motor cortex aids limb and digit positioning , 1992, Behavioural Brain Research.

[40]  I. Whishaw,et al.  Aphagia, behavior sequencing and body weight set point following orbital frontal lesions in rats , 1977, Physiology & Behavior.

[41]  S. Mackinnon,et al.  Choosing the correct functional assay: A comprehensive assessment of functional tests in the rat , 2005, Behavioural Brain Research.