Research report
Task specific adaptations in rat locomotion: Runway versus horizontal ladder

https://doi.org/10.1016/j.bbr.2005.11.017Get rights and content

Abstract

In walking quadrupeds the alternating activity pattern of antagonistic leg muscles and the coordination between legs is orchestrated by central pattern generating networks within the spinal cord. These networks are activated by tonic input from the reticular formation in the brainstem. Under more challenging conditions, such as walking on a horizontal ladder, successful locomotion relies upon additional context dependent input from pathways such as the cortico- and rubro-spinal tracts. In this study we used electromyographic and kinematic approaches to characterize the adaptations in the walking pattern in adult uninjured rats crossing a horizontal ladder. We found that the placement of a hind limb on a rung precisely followed the placement of the ipsilateral fore limb. This is different to normal walking where the hind limb is placed behind the position of the ipsilateral fore limb. The increased reach of the hind limbs is achieved by increased flexion of the hip and rotation of the pelvis during the swing phase. Electromyographic observations showed decreased burst duration in Tibialis anterior an ankle flexor muscle. Further changes in the muscle activity pattern were likely due to the reduced stepping frequency during ladder walking. Following a lesion of the dorsal column, containing major parts of the corticospinal tract, we found an increased number of stepping errors and changes in the stepping strategy. The step length of the fore limbs was reduced and the hind limbs were frequently positioned on rungs other than those occupied by the fore limb.

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)

Cited by (44)

  • Behavioral testing in animal models of spinal cord injury

    2020, Experimental Neurology
    Citation Excerpt :

    This makes it difficult to interpret the mechanism of recovery. To better differentiate between the restoration of descending function compared to pure spinal function, tests that challenge the motor system and require higher level functioning (brain and brainstem) can be applied (e.g., the horizontal ladder (Bolton et al., 2006; Metz and Whishaw, 2002) grid walk (Ma et al., 2001; Prakriya et al., 1993). or narrow beam test (Hicks and D'Amato, 1975).

  • Improved single pellet grasping using automated ad libitum full-time training robot

    2015, Behavioural Brain Research
    Citation Excerpt :

    Skilled motor tasks are effective research methods for studying the neural control of skilled movement and motor recovery after nervous system injury and disease [1–7]. At the present time there are a number of manually administered reaching and stepping tasks available for the study of forepaw movement in rodents including the Montoya staircase test [5,8,9], the well-grasping test [6,10], the Whishaw tray task [11], the horizontal ladder test [4,7,12], and the single pellet grasping (SPG) task [1]. However, it can be difficult and time consuming to train animals to perform many of these tasks.

  • The effect of a polyurethane-based reverse thermal gel on bone marrow stromal cell transplant survival and spinal cord repair

    2014, Biomaterials
    Citation Excerpt :

    Scores were averaged per experimental group. Sensorimotor function of the hindlimbs was assessed before (baseline) and at six weeks post-injection using horizontal ladder walking (n = 10/group) [7,41,42]. Slips of the foot and part of lower leg and slips of the full leg were counted and expressed as a percentage of the total number of steps.

View all citing articles on Scopus
View full text