Two chronic motor training paradigms differentially influence acute instrumental learning in spinally transected rats

Abstract

The effect of two chronic motor training paradigms on the ability of the lumbar spinal cord to perform an acute instrumental learning task was examined in neonatally (postnatal day 5; P5) spinal cord transected (i.e., spinal) rats. At approximately P30, rats began either unipedal hindlimb stand training (Stand-Tr; 20-25min/day, 5days/week), or bipedal hindlimb step training (Step-Tr; 20min/day; 5days/week) for 7 weeks. Non-trained spinal rats (Non-Tr) served as controls. After 7 weeks all groups were tested on the flexor-biased instrumental learning paradigm. We hypothesized that (1) Step-Tr rats would exhibit an increased capacity to learn the flexor-biased task relative to Non-Tr subjects, as locomotion involves repetitive training of the tibialis anterior (TA), the ankle flexor whose activation is important for successful instrumental learning, and (2) Stand-Tr rats would exhibit a deficit in acute motor learning, as unipedal training activates the ipsilateral ankle extensors, but not flexors. Results showed no differences in acute learning potential between Non-Tr and Step-Tr rats, while the Stand-Tr group showed a reduced capacity to learn the acute task. Further investigation of the Stand-Tr group showed that, while both the ipsilateral and contralateral hindlimbs were significantly impaired in their acute learning potential, the contralateral, untrained hindlimbs exhibited significantly greater learning deficits. These results suggest that different types of chronic peripheral input may have a significant impact on the ability to learn a novel motor task, and demonstrate the potential for experience-dependent plasticity in the spinal cord in the absence of supraspinal connectivity.

Fig. 1. Experimental Paradigm

All rats received a complete spinal cord transection at P5. Motor training began at P30 (see inset). (A) Typical electromyographic signals (EMG) obtained during body weight-supported (BWS) treadmill stepping (75% BWS at 13.5 cm/sec) from P5 spinally transected rats at ∼8-10 wks post-lesion showed alternating extensor (soleus; Sol) and flexor activation (tibialis anterior; TA) of both hindlimbs. (B) During unipedal hindlimb weight bearing at 75% BWS, the weight-bearing ankle extensor (Sol ipsi) and the non-weight-bearing ankle flexor (TA contra) muscles were recruited, while the ipsilateral TA and contralateral Sol were quiescent. a¹ and a² are calibrations for the Sol and TA EMG recordings during bipedal stepping, respectively; b¹ is the calibration for the EMG recordings for all muscles shown during unipedal standing. The experimental design and number of non-trained (Non-Tr), step-trained (Step-Tr), and stand-trained (Stand-Tr) subjects used for the acute instrumental learning test are also shown (see text for details). Ipsi refers to the ipsilateral hindlimb, and contra refers to the contralateral hindlimb.

Fig. 2. Instrumental learning in Non-Tr, Step-Tr, and Stand-Tr rats following 7 wks of step training or unilateral hindlimb stand training

The flexion duration (A) and the number of flexion responses (C) for each 1 min bin over 30 min of testing are shown, as are the overall average test flexion durations (B) and response numbers (D). For flexion duration, Non-Tr and Step-Tr groups were not significantly different, while the Stand-Tr flexion duration was significantly lower relative to both the Step-Tr and Non-Tr groups (B). The average number of flexion responses was not different between groups (D). Data are mean ± S.E.M. *; Significantly different at p < 0.05.

Fig. 3. Unilateral stand training induces a bilateral instrumental learning deficit

Non-Tr and Stand-Tr rats were tested for instrumental learning on both the ipsilateral and contralateral hindlimbs. The flexion duration (A) and the number of flexion responses (C) for each 1 min bin over 30 min of testing are shown, as are the overall average test durations (B) and response numbers (D). For within group analyses, flexion duration did not differ between the ipsilateral and contralateral hindlimbs of Non-Tr rats. In Stand-Tr rats, the contralateral hindlimbs learning showed a significant deficit relative to the ipsilateral hindlimbs (p < 0.05; A-B). Between groups, flexion duration was significantly lower in both the Stand-Tr ipsi and Stand-Tr contra limbs compared either hindlimb of the Non-Tr group (p < 0.05). Chronic motor training did not have a significant effect on the number of flexion responses within or between groups (C-D). Data are the mean ± S.E.M. *, Significantly different within groups at p < 0.05; ^, significantly different between groups at p < 0.05.