scholarly journals Acquisition of a simple motor skill: task-dependent adaptation and long-term changes in the human soleus stretch reflex

2019 ◽  
Vol 122 (1) ◽  
pp. 435-446 ◽  
Author(s):  
N. Mrachacz-Kersting ◽  
U. G. Kersting ◽  
P. de Brito Silva ◽  
Y. Makihara ◽  
L. Arendt-Nielsen ◽  
...  
Keyword(s):  
Operant Conditioning ◽  
Stretch Reflex ◽  
Conditioning Session ◽  
H Reflex ◽  
Reflex Change ◽  
Reflex Pathways ◽  
Term Change ◽  
Neurologically Normal ◽  
Spinal Stretch Reflex

Changing the H reflex through operant conditioning leads to CNS multisite plasticity and can affect previously learned skills. To further understand the mechanisms of this plasticity, we operantly conditioned the initial component (M1) of the soleus stretch reflex. Unlike the H reflex, the stretch reflex is affected by fusimotor control, comprises several bursts of activity resulting from temporally dispersed afferent inputs, and may activate spinal motoneurons via several different spinal and supraspinal pathways. Neurologically normal participants completed 6 baseline sessions and 24 operant conditioning sessions in which they were encouraged to increase (M1up) or decrease (M1down) M1 size. Five of eight M1up participants significantly increased M1; the final M1 size of those five participants was 143 ± 15% (mean ± SE) of the baseline value. All eight M1down participants significantly decreased M1; their final M1 size was 62 ± 6% of baseline. Similar to the previous H-reflex conditioning studies, conditioned reflex change consisted of within-session task-dependent adaptation and across-session long-term change. Task-dependent adaptation was evident in conditioning session 1 with M1up and by session 4 with M1down. Long-term change was evident by session 10 with M1up and by session 16 with M1down. Task-dependent adaptation was greater with M1up than with the previous H-reflex upconditioning. This may reflect adaptive changes in muscle spindle sensitivity, which affects the stretch reflex but not the H reflex. Because the stretch reflex is related to motor function more directly than the H reflex, M1 conditioning may provide a valuable tool for exploring the functional impact of reflex conditioning and its potential therapeutic applications. NEW & NOTEWORTHY Since the activity of stretch reflex pathways contributes to locomotion, changing it through training may improve locomotor rehabilitation in people with CNS disorders. Here we show for the first time that people can change the size of the soleus spinal stretch reflex through operant conditioning. Conditioned stretch reflex change is the sum of task-dependent adaptation and long-term change, consistent with H-reflex conditioning yet different from it in the composition and amount of the two components.

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.

Spinal and Supraspinal Effects of Long-Term Stimulation of Sensorimotor Cortex in Rats

2007 ◽  
Vol 98 (2) ◽  
pp. 878-887 ◽  
Author(s):  
Xiang Yang Chen ◽  
Shreejith Pillai ◽  
Yi Chen ◽  
Yu Wang ◽  
Lu Chen ◽  
...  
Keyword(s):  
Spinal Cord ◽  
Operant Conditioning ◽  
Sensorimotor Cortex ◽  
H Reflex ◽  
Freely Moving ◽  
Activity Dependent ◽  
Spinal Cord Function ◽  
The Brain ◽  
Stimulation Of

Sensorimotor cortex (SMC) modifies spinal cord reflex function throughout life and is essential for operant conditioning of the H-reflex. To further explore this long-term SMC influence over spinal cord function and its possible clinical uses, we assessed the effect of long-term SMC stimulation on the soleus H-reflex. In freely moving rats, the soleus H-reflex was measured 24 h/day for 12 wk. The soleus background EMG and M response associated with H-reflex elicitation were kept stable throughout. SMC stimulation was delivered in a 20-day-on/20-day-off/20-day-on protocol in which a train of biphasic 1-ms pulses at 25 Hz for 1 s was delivered every 10 s for the on-days. The SMC stimulus was automatically adjusted to maintain a constant descending volley. H-reflex size gradually increased during the 20 on-days, stayed high during the 20 off-days, and rose further during the next 20 on-days. In addition, the SMC stimulus needed to maintain a stable descending volley rose steadily over days. It fell during the 20 off-days and rose again when stimulation resumed. These results suggest that SMC stimulation, like H-reflex operant conditioning, induces activity-dependent plasticity in both the brain and the spinal cord and that the plasticity responsible for the H-reflex increase persists longer after the end of SMC stimulation than that underlying the change in the SMC response to stimulation.

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)

Operant conditioning of primate spinal reflexes: the H-reflex

1987 ◽  
Vol 57 (2) ◽  
pp. 443-459 ◽  
Author(s):  
J. R. Wolpaw
Keyword(s):  
Operant Conditioning ◽  
H Reflex ◽  
Spinal Reflexes ◽  
Triceps Surae ◽  
Spinal Reflex ◽  
Control Mode ◽  
Response Threshold ◽  
Reflex Amplitude ◽  
Emg Amplitude ◽  
Spinal Stretch Reflex

The study of primate memory substrates, the CNS alterations which preserve conditioned responses, requires an experimental model that fulfills two criteria. First, the essential alterations must be in a technically accessible location. Second, they must persist without input from other CNS regions. The spinal cord is the most technically accessible and readily isolated portion of the primate CNS. Recent work has demonstrated that the spinal stretch reflex (SSR), the initial, wholly segmental response to muscle stretch, can be operantly conditioned and suggests that this conditioning may produce persistent spinal alteration. The present study attempted similar operant conditioning of the H-reflex, the electrical analog of the SSR. The primary goals were to demonstrate that spinal reflex conditioning can occur even if the muscle spindle is removed from the reflex arc and to demonstrate conditioning in the lumbosacral cord, which is far preferable to the cervical cord for future studies of neuronal and synaptic mechanisms. Nine monkeys prepared with chronic fine-wire triceps surae (gastrocnemius and soleus) electromyographic (EMG) electrodes were taught by computer to maintain a given level of background EMG activity. At random times, a voltage pulse just above M response (direct muscle response) threshold was delivered to the posterior tibial nerve via a chronically implanted silicon nerve cuff and elicited the triceps surae H-reflex. Under the control mode, reward always followed. Under the HR increases or HR decreases mode, reward followed only if the absolute value of triceps surae EMG from 12 to 22 ms after the pulse (the H-reflex interval) was above (HR increases) or below (HR decreases) a set value. Monkeys completed 3,000-6,000 trials/day over study periods of 2-3 mo. Background EMG and M response amplitude remained stable throughout data collection. H-reflex amplitude remained stable under the control mode. Under the HR increases mode (5 animals) or HR decreases mode (4 animals), H-reflex amplitude (EMG amplitude in the H-reflex interval minus background EMG amplitude) changed appropriately over at least 6 wk. Change appeared to occur in two phases: an abrupt change within the first day, followed by slower change, which continued indefinitely. Change occurred in all three triceps surae muscles (medial and lateral gastrocnemii and soleus). Under the HR increases mode, H-reflex amplitude rose to an average of 213% of control, whereas under the HR decreases mode it fell to an average of 68% of control. The results demonstrate that the H-reflex can be operantly conditioned.(ABSTRACT TRUNCATED AT 400 WORDS)

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.

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.

H-Reflex Operant Conditioning in Mice

2006 ◽  
Vol 96 (4) ◽  
pp. 1718-1727 ◽  
Author(s):  
Jonathan S. Carp ◽  
Ann M. Tennissen ◽  
Xiang Yang Chen ◽  
Jonathan R. Wolpaw
Keyword(s):  
Spinal Cord ◽  
Operant Conditioning ◽  
Genetic Manipulation ◽  
H Reflex ◽  
Emg Activity ◽  
Conditioning Paradigm ◽  
Intramuscular Electrodes ◽  
Spinal Stretch Reflex ◽  
Simple Behavior

Rats, monkeys, and humans can alter the size of their spinal stretch reflex and its electrically induced analog, the H-reflex (HR), when exposed to an operant conditioning paradigm. Because this conditioning induces plasticity in the spinal cord, it offers a unique opportunity to identify the neuronal sites and mechanisms that underlie a well-defined change in a simple behavior. To facilitate these studies, we developed an HR operant conditioning protocol in mice, which are better suited to genetic manipulation and electrophysiological spinal cord study in vitro than rats or primates. Eleven mice under deep surgical anesthesia were implanted with tibial nerve stimulating electrodes and soleus and gastrocnemius intramuscular electrodes for recording ongoing and stimulus-evoked EMG activity. During the 24-h/day computer-controlled experiment, mice received a liquid reward for either increasing (up-conditioning) or decreasing (down-conditioning) HR amplitude while maintaining target levels of ongoing EMG and directly evoked EMG (M-responses). After 3–7 wk of conditioning, the HR amplitude was 133 ± 7% (SE) of control for up-conditioning and 71 ± 8% of control for down-conditioning. HR conditioning was successful (i.e., ≥20% change in HR amplitude in the appropriate direction) in five of six up-conditioned animals (mean final HR amplitude = 139 ± 5% of control HR for successful mice) and in four of five down-conditioned animals (mean final HR amplitude = 63 ± 8% of control HR for successful mice). These effects were not attributable to differences in the net level of motoneuron pool excitation, stimulation strength, or distribution of HR trials throughout the day. Thus mice exhibit HR operant conditioning comparable with that observed in rats and monkeys.

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