Research reportTask specific adaptations in rat locomotion: Runway versus horizontal ladder
Introduction
Walking in quadrupeds is characterized by a rhythmic alternation of flexor and extensor muscles of the limbs. This pattern is orchestrated by neuronal networks within the spinal cord collectively referred to as central pattern generators (CPGs) [1], [2] that are activated by tonic input from the reticulospinal tract [3], [4]. The existence of spinal CPGs and the diffusely projecting reticulospinal tract fibers throughout the ventral and lateral funiculus of the spinal cord can explain why stepping movements can still be elicited after severe but incomplete spinal cord injuries in animal models [5], [6], [7], [8]. Rats are often used to model spinal cord injury (SCI) and although the walking pattern is coordinated by CPGs in the lower spinal cord (and thus not necessarily reflecting the integrity of experimentally injured spinal tracts) hind limb function during walking is a common functional readout. To quantify the walking performance several approaches have been employed including visual rating scales of open field locomotion [9], or other more specific measures including footprint analysis [10], [11], [12], kinematic analysis and electromyographic recordings [13]. These approaches however focus on stereotyped walking on a flat surface. As described above, the drawback of focusing on stereotyped walking is that with spinal circuitry dictating the basic walking pattern, the interpretation of functional outcome due to treatment becomes difficult. An alternative approach in locomotor assessment is to study skilled walking as it relies upon the additional contribution of pathways such as the cortico- (CST) and rubro-spinal tract (RST). Lesions to these pathways result in pronounced and permanent deficits when environmental challenges are imposed [14], [15]. Their relatively distinct projection pattern makes RST and CST popular choices for studies of SCI, and the evaluation of skilled walking allows for a greater connection between the function and integrity of these tracts.
While skilled walking can be assessed using error counts without a detailed evaluation of the movement itself [8], [16], [17], analyzing the walking pattern in greater depth gives the opportunity to observe otherwise undetectable subtle features and adjustments possibly controlled by input from the CST and RST. For example, adjustments following various spinal cord lesions have been revealed in the walking pattern of rats as expressed through ground reaction forces [15], [18] or electromyographic recordings during rat treadmill locomotion [19]. Metz and Whishaw [14] used video analysis to provide a qualitative assessment of locomotion on a horizontal ladder; however quantitative measures such as comparison of joint angles have not been reported. These measures along with electromyography can possibly provide insight into fine motor control during walking and may offer a link between functional performance and the integrity of descending tracts responsible for skilled locomotion (i.e., CST and RST).
The present study examines healthy rats walking over a flat runway or a horizontal ladder while EMG activity and kinematic data were recorded to profile both forms of locomotion in detail and identify key variables of distinction. Subsequently, the strategies of ladder walking in healthy rats and rats with a dorsal column lesion were compared.
Section snippets
Methods
Experiments were conducted using 10 adult female Lewis rats (180–200 g; five with and five without spinal cord lesion) in which EMG electrodes were surgically implanted (see below). All rats were kept at a 12:12 h light dark cycle with water and food provided ad libitum. This study was conducted in accordance with the Canadian Council on Animal Care guidelines and policies with approval from the Health Sciences Animal Policy and Welfare Committee for the University of Alberta. Rats were trained
General observations
Rats generally cross the 1 m long horizontal ladder slower than the same distance on a flat runway. Based on EMG analysis (which has a higher time resolution than the kinematic analysis) the average step cycle duration (out of 10 steps of each rat; ±S.D.) was 537 ms ± 57 when walking on the ladder and 329 ms ± 85 when walking on the runway. The average stride length out of 15 steps/animal was 12.4 cm ± 0.4 during runway walking, which was significantly longer than in rats walking on the horizontal ladder
Discussion
The present study compared walking in adult rats under two conditions representing different levels of motor complexity: walking on a smooth surface coordinated mainly by neuronal circuits within the spinal cord [21] and walking on a horizontal ladder, a task that necessitates additional descending input [14], [18]. In a second experiment descending input was reduced by a lesion of the dorsal column, thereby ablating the major projection of the CST.
An important aspect of the interpretation of
Acknowledgements
We would like to thank R. Vavrek for technical support. The study was supported by the Alberta Heritage Foundation for Medical Research and the International Spinal Research Trust.
References (22)
- et al.
Locomotor recovery following subtotal spinal cord lesions in a rat model
Neurosci Lett
(1988) - et al.
Localization of a descending pathway in the spinal cord which is necessary for controlled treadmill locomotion
Neurosci Lett
(1980) Anatomical correlates of locomotor recovery following dorsal and ventral lesions of the rat spinal cord
Exp Neurol
(2002)- et al.
An index of the functional condition of rat sciatic nerve based on measurements made from walking tracks
Exp Neurol
(1982) - et al.
Methods to assess the development and recovery of locomotor function after spinal cord injury in rats
Exp Neurol
(1993) Efficient testing of motor function in spinal cord injured rats
Brain Res
(2000)- et al.
Cortical and subcortical lesions impair skilled walking in the ladder rung walking test: a new task to evaluate fore- and hindlimb stepping, placing, and co-ordination
J Neurosci Methods
(2002) Adult rat forelimb dysfunction after dorsal cervical spinal cord injury
Exp Neurol
(2005)Collagen containing neurotrophin-3 (NT-3) attracts regrowing injured corticospinal axons in the adult rat spinal cord and promotes partial functional recovery
Exp Neurol
(1998)- et al.
Complete locomotor recovery following corticospinal tract lesions: measurement of ground reaction forces during overground locomotion in rats
Behav Brain Res
(1999)
The activation of back muscles during locomotion in the developing rat
Brain Res Dev
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