Conditioned H-Reflex Increase Persists After Transection of the Main Corticospinal Tract in Rats

2003 ◽  
Vol 90 (5) ◽  
pp. 3572-3578 ◽  
Author(s):  
Xiang Yang Chen ◽  
Lu Chen ◽  
Jonathan R. Wolpaw
Keyword(s):  
Spinal Cord ◽  
Operant Conditioning ◽  
Corticospinal Tract ◽  
Dorsal Column ◽  
H Reflex ◽  
Initial Value ◽  
Cord Injury ◽  
Training Mode ◽  
The Right ◽  
Spinal Stretch Reflex

The brain shapes spinal cord function throughout life. Operant conditioning of the H-reflex, the electrical analog of the spinal stretch reflex (SSR), is a relatively simple model for exploring the spinal cord plasticity underlying this functional change and may provide a new method for modifying spinal cord reflexes after spinal cord injury. In response to an operant conditioning protocol, rats can gradually increase (i.e., up-training mode) or decrease (i.e., down-training mode) the soleus H-reflex. This study explored the effects of midthoracic transection of the ipsilateral lateral column (LC) (rubrospinal, vestibulospinal, and reticulospinal tracts), the dorsal column corticospinal tract (CST), or the dorsal column ascending tract (DA) on maintenance of an H-reflex increase that has already occurred. Rats were implanted with EMG electrodes in the right soleus muscle and a nerve-stimulating cuff on the right posterior tibial nerve. After initial (i.e., control) H-reflex size was determined, the rats were exposed for 50 days to the up-training mode, in which reward was given when the H-reflex was above a criterion value. H-reflex size gradually rose to 168 ± 12% (mean ± SE) of its initial value. Each rat then received an LC, CST, or DA transection and continued under the up-training mode for 50 more days. None of the transections abolished the H-reflex increase. H-reflex size increased further to 197 ± 19% of its initial value and did not differ significantly among LC, CST, and DA rats ( P > 0.78 by ANOVA). Although earlier studies show that the main CST is needed for acquisition of H-reflex up-training and down-training and for maintenance of down-training, this study shows that it is not needed for maintenance of up-training. It adds to the evidence that H-reflex conditioning changes the spinal cord and that the spinal cord plasticity associated with up-training is different from that associated with down-training.

Dorsal Column But Not Lateral Column Transection Prevents Down-Conditioning of H Reflex in Rats

1997 ◽  
Vol 78 (3) ◽  
pp. 1730-1734 ◽  
Author(s):  
Xiang Yang Chen ◽  
Jonathan R. Wolpaw
Keyword(s):  
Spinal Cord ◽  
Corticospinal Tract ◽  
Dorsal Column ◽  
H Reflex ◽  
Transient Effects ◽  
Sprague Dawley ◽  
Initial Value ◽  
Lateral Column ◽  
The Right ◽  
Spinal Stretch Reflex

Chen, Xiang Yang and Jonathan R. Wolpaw. Dorsal column but not lateral column transection prevents down-conditioning of H reflex in rats. J. Neurophysiol. 78: 1730–1734, 1997. Operant conditioning of the H reflex, the electrical analogue of the spinal stretch reflex, in freely moving rats is a relatively simple model for studying long-term supraspinal control over spinal cord function. Motivated by food reward, rats can gradually increase or decrease the soleus H reflex. This study is the first effort to determine which spinal cord pathways convey the descending influence from supraspinal structures that changes the H reflex. In anesthetized Sprague-Dawley rats, the entire dorsal column (DC), which includes the main corticospinal tract, or the right lateral column (LC) was transected by electrocautery. Animals recovered quickly and the minimal transient effects of transection on the right soleus H reflex disappeared within 16 days. Beginning at least 18 days after transection, 12 rats were exposed to the HRdown-conditioning mode, in which reward was given when the H reflex of the right soleus muscle was below a criterion value. In seven LC rats exposed to the HRdown mode, the H reflex fell to 71 ± 8% (mean ± SE) of its initial value. In six of the seven, conditioning was successful (i.e., decrease to ≤80%). These results were comparable with those previously obtained from normal rats. In contrast, in five DC rats exposed to the HRdown mode, the H reflex at the end of exposure was 106 ± 12% of its initial value. In none of these rats was HRdown-conditioning successful. DC rats differed significantly from normal and LC rats in both final H reflex values and number successful. In five DC and three LC rats that continued under control conditions over 30–78 days, the H reflex at the end of the period was 98 ± 4% and 100 ± 8%, respectively, of its initial value, indicating that DC or LC transection itself did not lead to gradual increase or decrease in the H reflex. The results indicate that the DC, containing the main corticospinal tract, is essential for HRdown-conditioning, whereas the ipsilateral LC, containing the main rubrospinal, vestibulospinal, and reticulospinal tracts, is not essential. Combined with the known muscular specificity of conditioning, these results suggest that the main corticospinal tract is essential for HRdown-conditioning. The DC ascending tract might also be necessary. The respective roles of the DC descending and ascending tracts, and transection effects on HRup-conditioning and on the maintenance of both HRup- and HRdown-conditioning after they have occurred, remain to be defined.

Probable Corticospinal Tract Control of Spinal Cord Plasticity in the Rat

2002 ◽  
Vol 87 (2) ◽  
pp. 645-652 ◽  
Author(s):  
Xiang Yang Chen ◽  
Jonathan R. Wolpaw
Keyword(s):  
Spinal Cord ◽  
Corticospinal Tract ◽  
Recovery Of Function ◽  
Dorsal Column ◽  
H Reflex ◽  
Sprague Dawley ◽  
Lateral Column ◽  
Gradual Loss ◽  
Cord Injury ◽  
Spinal Stretch Reflex

Descending activity from the brain shapes spinal cord reflex function throughout life, yet the mechanisms responsible for this spinal cord plasticity are poorly understood. Operant conditioning of the H-reflex, the electrical analogue of the spinal stretch reflex, is a simple model for investigating these mechanisms. An earlier study in the Sprague-Dawley rat showed that acquisition of an operantly conditioned decrease in the soleus H-reflex is not prevented by mid-thoracic transection of the ipsilateral lateral column (LC), which contains the rubrospinal, reticulospinal, and vestibulospinal tracts, and is prevented by transection of the dorsal column, which contains the main corticospinal tract (CST) and the dorsal column ascending tract (DA). The present study explored the effects of CST or DA transection on acquisition of an H-reflex decrease, and the effects of LC, CST, or DA transection on maintenance of an established decrease. CST transection prior to conditioning prevented acquisition of H-reflex decrease, while DA transection did not do so. CST transection after H-reflex decrease had been acquired led to gradual loss of the decrease over 10 days, and resulted in an H-reflex that was significantly larger than the original, naive H-reflex. In contrast, LC or DA transection after H-reflex decrease had been acquired did not affect maintenance of the decrease. These results, in combination with the earlier study, strongly imply that in the rat the corticospinal tract (CST) is essential for acquisition and maintenance of operantly conditioned decrease in the H-reflex and that other major spinal cord pathways are not essential. This previously unrecognized aspect of CST function gives insight into the processes underlying acquisition and maintenance of motor skills and could lead to novel methods for inducing, guiding, and assessing recovery of function after spinal cord injury.

scholarly journals Operant Conditioning of Reciprocal Inhibition in Rat Soleus Muscle

2006 ◽  
Vol 96 (4) ◽  
pp. 2144-2150 ◽  
Author(s):  
Xiang Yang Chen ◽  
Lu Chen ◽  
Yi Chen ◽  
Jonathan R. Wolpaw
Keyword(s):  
Spinal Cord ◽  
Operant Conditioning ◽  
Reciprocal Inhibition ◽  
H Reflex ◽  
Spinal Reflex ◽  
Sprague Dawley ◽  
Sprague Dawley Rats ◽  
Cord Injury ◽  
Rat Soleus Muscle ◽  
Spinal Stretch Reflex

Operant conditioning of the H-reflex, the electrical analog of the spinal stretch reflex (SSR), induces activity-dependent plasticity in the spinal cord and might be used to improve locomotion after spinal cord injury. To further assess the potential clinical significance of spinal reflex conditioning, this study asks whether another well-defined spinal reflex pathway, the disynaptic pathway underlying reciprocal inhibition (RI), can also be operantly conditioned. Sprague-Dawley rats were implanted with electromyographic (EMG) electrodes in right soleus (SOL) and tibialis anterior (TA) muscles and a stimulating cuff on the common peroneal (CP) nerve. When background EMG in both muscles remained in defined ranges, CP stimulation elicited the TA H-reflex and SOL RI. After collection of control data for 20 days, each rat was exposed for 50 days to up-conditioning (RIup mode) or down-conditioning (RIdown mode) in which food reward occurred if SOL RI evoked by CP stimulation was more (RIup mode) or less (RIdown mode) than a criterion. TA and SOL background EMG and TA M response remained stable. In every rat, RI conditioning was successful (i.e., change ≥20% in the correct direction). In the RIup rats, final SOL RI averaged 171± 28% (mean ± SE) of control, and final TA H-reflex averaged 114 ± 14%. In the RIdown rats, final SOL RI averaged 37 ± 13% of control, and final TA H-reflex averaged 60 ± 18%. Final SOL RI and TA H-reflex sizes were significantly correlated. Thus like the SSR and the H-reflex, RI can be operantly conditioned; and conditioning one reflex can affect another reflex as well.

scholarly journals Dendritic spine dysgenesis contributes to hyperreflexia after spinal cord injury

2015 ◽  
Vol 113 (5) ◽  
pp. 1598-1615 ◽  
Author(s):  
Samira P. Bandaru ◽  
Shujun Liu ◽  
Stephen G. Waxman ◽  
Andrew M. Tan
Keyword(s):  
Spinal Cord ◽  
Spinal Cord Injury ◽  
Motor Neurons ◽  
Dendritic Spine ◽  
Specific Inhibitor ◽  
H Reflex ◽  
Spine Density ◽  
Sprague Dawley ◽  
Cord Injury ◽  
Spinal Stretch Reflex

Hyperreflexia and spasticity are chronic complications in spinal cord injury (SCI), with limited options for safe and effective treatment. A central mechanism in spasticity is hyperexcitability of the spinal stretch reflex, which presents symptomatically as a velocity-dependent increase in tonic stretch reflexes and exaggerated tendon jerks. In this study we tested the hypothesis that dendritic spine remodeling within motor reflex pathways in the spinal cord contributes to H-reflex dysfunction indicative of spasticity after contusion SCI. Six weeks after SCI in adult Sprague-Dawley rats, we observed changes in dendritic spine morphology on α-motor neurons below the level of injury, including increased density, altered spine shape, and redistribution along dendritic branches. These abnormal spine morphologies accompanied the loss of H-reflex rate-dependent depression (RDD) and increased ratio of H-reflex to M-wave responses (H/M ratio). Above the level of injury, spine density decreased compared with below-injury spine profiles and spine distributions were similar to those for uninjured controls. As expected, there was no H-reflex hyperexcitability above the level of injury in forelimb H-reflex testing. Treatment with NSC23766, a Rac1-specific inhibitor, decreased the presence of abnormal dendritic spine profiles below the level of injury, restored RDD of the H-reflex, and decreased H/M ratios in SCI animals. These findings provide evidence for a novel mechanistic relationship between abnormal dendritic spine remodeling in the spinal cord motor system and reflex dysfunction in SCI.

scholarly journals Wallerian degeneration in cervical spinal cord tracts is commonly seen in routine T2-weighted MRI after traumatic spinal cord injury and is associated with impairment in a retrospective study

2020 ◽  
Author(s):  
Tim Fischer ◽  
Christoph Stern ◽  
Patrick Freund ◽  
Martin Schubert ◽  
Reto Sutter
Keyword(s):  
Spinal Cord ◽  
Spinal Cord Injury ◽  
Wallerian Degeneration ◽  
Evoked Potential ◽  
Corticospinal Tract ◽  
Cervical Spinal Cord ◽  
Dorsal Column ◽  
Traumatic Spinal Cord Injury ◽  
Spinothalamic Tract ◽  
Cord Injury

Abstract Objectives Wallerian degeneration (WD) is a well-known process after nerve injury. In this study, occurrence of remote intramedullary signal changes, consistent with WD, and its correlation with clinical and neurophysiological impairment were assessed after traumatic spinal cord injury (tSCI). Methods In 35 patients with tSCI, WD was evaluated by two radiologists on T2-weighted images of serial routine MRI examinations of the cervical spine. Dorsal column (DC), lateral corticospinal tract (CS), and lateral spinothalamic tract (ST) were the analyzed anatomical regions. Impairment scoring according to the American Spinal Injury Association Impairment Scale (AIS, A–D) as well as a scoring system (0–4 points) for motor evoked potential (MEP) and sensory evoked potential (SEP) was included. Mann-Whitney U test was used to test for differences. Results WD in the DC occurred in 71.4% (n = 25), in the CS in 57.1% (n = 20), and in 37.1% (n = 13) in the ST. With WD present, AIS grades were worse for all tracts. DC: median AIS B vs D, p < 0.001; CS: B vs D, p = 0.016; and ST: B vs D, p = 0.015. More pathological MEP scores correlated with WD in the DC (median score 0 vs 3, p < 0.001) and in the CS (0 vs 2, p = 0.032). SEP scores were lower with WD in the DC only (1 vs 2, p = 0.031). Conclusions WD can be detected on T2-weighted scans in the majority of cervical spinal cord injury patients and should be considered as a direct effect of the trauma. When observed, it is associated with higher degree of impairment. Key Points • Wallerian degeneration is commonly seen in routine MRI after traumatic spinal cord injury. • Wallerian degeneration is visible in the anatomical regions of the dorsal column, the lateral corticospinal tract, and the lateral spinothalamic tract. • Presence of Wallerian degeneration is associated with higher degree of impairment.

Operant conditioning of H-reflex in freely moving rats

1995 ◽  
Vol 73 (1) ◽  
pp. 411-415 ◽  
Author(s):  
X. Y. Chen ◽  
J. R. Wolpaw
Keyword(s):  
Operant Conditioning ◽  
H Reflex ◽  
Response Amplitude ◽  
Primate Research ◽  
Sprague Dawley ◽  
Initial Value ◽  
Reflex Amplitude ◽  
Nerve Cuff ◽  
Spinal Stretch Reflex ◽  
Experimental Use

1. Primates can increase or decrease the spinal stretch reflex and its electrical analogue, the H-reflex (HR), in response to an operant conditioning task. This conditioning changes the spinal cord itself and thereby provides an experimental model for defining the processes and substrates of a learned change in behavior. Because the phenomenon has been demonstrated only in primates, its generality and theoretical implications remain unclear, and its experimental use is restricted by the difficulties of primate research. In response to these issues, the present study explored operant conditioning of the H-reflex in the rat. 2. Seventeen Sprague-Dawley rats implanted with chronic electromyographic (EMG) recording electrodes in one soleus muscle and nerve cuff stimulating electrodes on the posterior tibial nerve were rewarded (either with medial forebrain bundle stimulation or food) for increasing (HRup conditioning mode) or decreasing (HRdown conditioning mode) soleus H-reflex amplitude without change in background EMG or M response (direct muscle response) amplitude. 3. H-reflex amplitude changed appropriately over 3-4 wk. Under the HRup mode, it rose to an average of 158 +/- 54% (mean +/- SD) of initial value, whereas under the HRdown mode it fell to an average of 67 +/- 11% of initial value. Background EMG and M response amplitude did not change. 4. Operant conditioning of the H-reflex in the rat appears similar in rate and final magnitude of change to that observed in the monkey.(ABSTRACT TRUNCATED AT 250 WORDS)

Memory traces in primate spinal cord produced by operant conditioning of H-reflex

1989 ◽  
Vol 61 (3) ◽  
pp. 563-572 ◽  
Author(s):  
J. R. Wolpaw ◽  
C. L. Lee
Keyword(s):  
Spinal Cord ◽  
Operant Conditioning ◽  
Internal Control ◽  
H Reflex ◽  
Triceps Surae ◽  
Reflex Response ◽  
Reflex Amplitude ◽  
Memory Traces ◽  
Spinal Stretch Reflex ◽  
Root Stimulation

1. Study of memory traces in higher animals requires experimental models possessing well-localized and technically accessible memory traces--plasticity responsible for behavioral change, not dependent on control from elsewhere, and open to detailed investigation. Our purpose has been to develop such a model based on the wholly spinal, largely monosynaptic path of the spinal stretch reflex. Previous studies described operant conditioning of this reflex and of its electrical analog, the H-reflex. In this study, we sought to determine whether conditioning causes changes in the spinal cord that affect the reflex and are not dependent on continued supraspinal influence, and thus qualify as memory traces. 2. Sixteen monkeys underwent chronic conditioning of the triceps surae H-reflex. Eight were rewarded for increasing H-reflex amplitude (HR increases mode), and eight were rewarded for decreasing it (HR decreases mode). In each animal, the other leg was an internal control. Over several months of conditioning, H-reflex amplitude in the conditioned leg rose in HR increases animals and fell in HR decreases animals. H-reflex amplitude in the control leg changed little. 3. After HR increases or HR decreases conditioning, each animal was deeply anesthetized and surgically prepared. The reflex response to supramaximal dorsal root stimulation was measured from the triceps surae nerve as percent of response to supramaximal ventral root stimulation, which was the maximum possible response. Data from both legs were collected before and for up to 3 days after thoracic (T9-10) cord transection. The animal remained deeply anesthetized throughout and was killed by overdose. 4. The reflex asymmetries produced by conditioning were still present several days after transection removed supraspinal influence: reflexes of HR increases animals were significantly larger in HR increases legs than in control legs and reflexes of HR decreases animals were significantly smaller in HR decreases legs than in control legs. 5. Reflex amplitude was much greater in the control legs of anesthetized HR decreases animals than in the control legs of anesthetized HR increases animals. 6. Chronic conditioning had at least two effects on the spinal cord. The first effect, task-appropriate reflex asymmetry, was evident both in the awake behaving animal and in the anesthetized transected animal. The second effect, larger control leg reflexes in HR decreases than in HR increases animals, was evident only in the anesthetized animal. By removing supraspinal control, anesthesia and transection revealed a previously hidden effect of conditioning.(ABSTRACT TRUNCATED AT 400 WORDS)

scholarly journals Persistent beneficial impact of H-reflex conditioning in spinal cord-injured rats

2014 ◽  
Vol 112 (10) ◽  
pp. 2374-2381 ◽  
Author(s):  
Yi Chen ◽  
Lu Chen ◽  
Yu Wang ◽  
Jonathan R. Wolpaw ◽  
Xiang Yang Chen
Keyword(s):  
Spinal Cord ◽  
H Reflex ◽  
Spinal Reflex ◽  
Spinal Cord Regeneration ◽  
Lateral Column ◽  
Beneficial Effects ◽  
Cord Injury ◽  
Beneficial Impact ◽  
The Right ◽  
Spinal Cord Injured

Operant conditioning of a spinal cord reflex can improve locomotion in rats and humans with incomplete spinal cord injury. This study examined the persistence of its beneficial effects. In rats in which a right lateral column contusion injury had produced asymmetric locomotion, up-conditioning of the right soleus H-reflex eliminated the asymmetry while down-conditioning had no effect. After the 50-day conditioning period ended, the H-reflex was monitored for 100 [±9 (SD)] (range 79–108) more days and locomotion was then reevaluated. After conditioning ended in up-conditioned rats, the H-reflex continued to increase, and locomotion continued to improve. In down-conditioned rats, the H-reflex decrease gradually disappeared after conditioning ended, and locomotion at the end of data collection remained as impaired as it had been before and immediately after down-conditioning. The persistence (and further progression) of H-reflex increase but not H-reflex decrease in these spinal cord-injured rats is consistent with the fact that up-conditioning improved their locomotion while down-conditioning did not. That is, even after up-conditioning ended, the up-conditioned H-reflex pathway remained adaptive because it improved locomotion. The persistence and further enhancement of the locomotor improvement indicates that spinal reflex conditioning protocols might supplement current therapies and enhance neurorehabilitation. They may be especially useful when significant spinal cord regeneration becomes possible and precise methods for retraining the regenerated spinal cord are needed.

scholarly journals Locomotor impact of beneficial or nonbeneficial H-reflex conditioning after spinal cord injury

2014 ◽  
Vol 111 (6) ◽  
pp. 1249-1258 ◽  
Author(s):  
Yi Chen ◽  
Lu Chen ◽  
Rongliang Liu ◽  
Yu Wang ◽  
Xiang Yang Chen ◽  
...  
Keyword(s):  
Spinal Cord ◽  
H Reflex ◽  
Spinal Reflex ◽  
Step Cycle ◽  
Reflex Pathway ◽  
Cord Injury ◽  
Kinematic Analyses ◽  
Spinal Cord Contusion ◽  
The Right ◽  
The Impact

When new motor learning changes neurons and synapses in the spinal cord, it may affect previously learned behaviors that depend on the same spinal neurons and synapses. To explore these effects, we used operant conditioning to strengthen or weaken the right soleus H-reflex pathway in rats in which a right spinal cord contusion had impaired locomotion. When up-conditioning increased the H-reflex, locomotion improved. Steps became longer, and step-cycle asymmetry (i.e., limping) disappeared. In contrast, when down-conditioning decreased the H-reflex, locomotion did not worsen. Steps did not become shorter, and asymmetry did not increase. Electromyographic and kinematic analyses explained how H-reflex increase improved locomotion and why H-reflex decrease did not further impair it. Although the impact of up-conditioning or down-conditioning on the H-reflex pathway was still present during locomotion, only up-conditioning affected the soleus locomotor burst. Additionally, compensatory plasticity apparently prevented the weaker H-reflex pathway caused by down-conditioning from weakening the locomotor burst and further impairing locomotion. The results support the hypothesis that the state of the spinal cord is a “negotiated equilibrium” that serves all the behaviors that depend on it. When new learning changes the spinal cord, old behaviors undergo concurrent relearning that preserves or improves their key features. Thus, if an old behavior has been impaired by trauma or disease, spinal reflex conditioning, by changing a specific pathway and triggering a new negotiation, may enable recovery beyond that achieved simply by practicing the old behavior. Spinal reflex conditioning protocols might complement other neurorehabilitation methods and enhance recovery.

scholarly journals Operant conditioning of the soleus H-reflex does not induce long-term changes in the gastrocnemius H-reflexes and does not disturb normal locomotion in humans

2014 ◽  
Vol 112 (6) ◽  
pp. 1439-1446 ◽  
Author(s):  
Yukiko Makihara ◽  
Richard L. Segal ◽  
Jonathan R. Wolpaw ◽  
Aiko K. Thompson
Keyword(s):  
Operant Conditioning ◽  
H Reflex ◽  
Emg Activity ◽  
Term Change ◽  
Cord Injury ◽  
Long Term Changes ◽  
Normal Humans ◽  
Spinal Stretch Reflex ◽  
The Impact

In normal animals, operant conditioning of the spinal stretch reflex or the H-reflex has lesser effects on synergist muscle reflexes. In rats and people with incomplete spinal cord injury (SCI), soleus H-reflex operant conditioning can improve locomotion. We studied in normal humans the impact of soleus H-reflex down-conditioning on medial (MG) and lateral gastrocnemius (LG) H-reflexes and on locomotion. Subjects completed 6 baseline and 30 conditioning sessions. During conditioning trials, the subject was encouraged to decrease soleus H-reflex size with the aid of visual feedback. Every sixth session, MG and LG H-reflexes were measured. Locomotion was assessed before and after conditioning. In successfully conditioned subjects, the soleus H-reflex decreased 27.2%. This was the sum of within-session (task dependent) adaptation (13.2%) and across-session (long term) change (14%). The MG H-reflex decreased 14.5%, due mainly to task-dependent adaptation (13.4%). The LG H-reflex showed no task-dependent adaptation or long-term change. No consistent changes were detected across subjects in locomotor H-reflexes, EMG activity, joint angles, or step symmetry. Thus, in normal humans, soleus H-reflex down-conditioning does not induce long-term changes in MG/LG H-reflexes and does not change locomotion. In these subjects, task-dependent adaptation of the soleus H-reflex is greater than it is in people with SCI, whereas long-term change is less. This difference from results in people with SCI is consistent with the fact that long-term change is beneficial in people with SCI, since it improves locomotion. In contrast, in normal subjects, long-term change is not beneficial and may necessitate compensatory plasticity to preserve satisfactory locomotion.

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