Adaptive plasticity in primate spinal stretch reflex: initial development

1983 ◽  
Vol 50 (6) ◽  
pp. 1296-1311 ◽  
Author(s):  
J. R. Wolpaw ◽  
D. J. Braitman ◽  
R. F. Seegal

Description of the neuronal and synaptic bases of memory in the vertebrate central nervous system (CNS) requires a CNS stimulus-response pathway that is defined and accessible, has the capacity for adaptive change, and clearly contains the responsible substrates. This study was an attempt to determine whether the spinal stretch reflex (SSR), the initial, purely spinal, portion of the muscle stretch response, which satisfies the first requirement, also satisfies the second, capacity for adaptive change. Monkeys prepared with chronic fine-wire biceps electromyographic (EMG) electrodes were trained to maintain elbow position and a given level of biceps background EMG activity against constant extension torque. At random times, a brief additional extension torque pulse extended the elbow and elicited the biceps SSR. Under the control mode, reward always followed. Under the SSR increases or SSR decreases mode, reward followed only if the absolute value of biceps EMG from 14 to 24 ms after stretch onset (the SSR interval) was above or below a set value. Animals performed 3,000-6,000 trials/day over data-collection periods of up to 15 mo. Background EMG and the initial 30 ms of pulse-induced extension remained stable throughout data collection. Under the SSR increases or SSR decreases mode, SSR amplitude (EMG amplitude in the SSR interval minus background EMG amplitude) changed appropriately. Change was evident in 5-10 days and progressed over at least 4 wk. The SSR increased (SSR increases) to 140-190% control amplitude or decreased (SSR decreases) to 22-79%. SSR change did not regress over 12-day gaps in task performance. A second pair of biceps electrodes, monitored simultaneously, supplied comparable data, indicating that SSR amplitude change occurred throughout the muscle. Beyond 40 ms after pulse onset, elbow extension was inversely correlated with SSR amplitude. The delay between the SSR and its apparent effect on movement is consistent with expected motor-unit contraction time. The data demonstrate that the SSR is capable of adaptive change. At present the most likely site(s) of the mechanism of SSR amplitude change are the Ia synapse and/or the muscle spindle. Available related evidence suggests persistent segmental change may in fact come to mediate SSR amplitude change. If so, such segmental change would constitute a technically accessible fragment of a memory.

1986 ◽  
Vol 55 (2) ◽  
pp. 272-279 ◽  
Author(s):  
J. R. Wolpaw ◽  
J. A. O'Keefe ◽  
P. A. Noonan ◽  
M. G. Sanders

Monkeys can gradually change the amplitude of the wholly segmental, largely monosynaptic, spinal stretch reflex (SSR) when confronted by a task requiring such change (15-19). Change develops over months and may reverse and redevelop at similarly slow rates. We investigated the persistence of SSR amplitude change over nonperformance periods of up to 38 days. Eight animals with chronic EMG electrodes learned to maintain elbow angle and a given level of biceps background EMG against constant extension torque. At random times, a brief additional extension torque pulse elicited the biceps SSR. In the control mode, reward always followed. Under the SSR increase or SSR decrease mode, reward occurred only if the absolute value of biceps EMG in the SSR interval was above or below a set value. Animals completed 3,000-6,000 trials/day over data-collection periods of 2-17 mo. Animals worked first under the control mode for up to 60 days and then under the SSR increase or SSR decrease mode for up to 274 days. Mode was switched once or twice more (SSR increase to SSR decrease or vice versa) over subsequent months. Animals responded to each SSR increase or SSR decrease mode exposure with gradual mode-appropriate change in SSR amplitude. Mode exposures were interrupted by gaps in performance of 10-38 days. Gaps produced transient 10- to 15% decreases in SSR amplitude under the control mode. This nonspecific decrease disappeared over the first week of postgap performance. Under the control mode, gaps had no other effects on SSR amplitude.(ABSTRACT TRUNCATED AT 250 WORDS)


1983 ◽  
Vol 50 (6) ◽  
pp. 1312-1319 ◽  
Author(s):  
J. R. Wolpaw ◽  
R. F. Seegal ◽  
J. A. O'Keefe

Monkeys can gradually change the amplitude of the biceps spinal stretch reflex (SSR) without change in initial muscle length or biceps background electromyographic activity (EMG) (17). We investigated the concurrent behavior of synergist (brachialis and brachioradialis) and antagonist (triceps) muscles. Synergist background EMG remained stable while marked change occurred in biceps SSR amplitude. Triceps background EMG was minimal under all conditions. Thus biceps SSR amplitude change was not due to change in the background activity of closely related muscles. When biceps SSR amplitude changed, synergist SSR amplitude changed similarly but to a lesser extent. Brachialis change averaged 72% of biceps change, while brachioradialis change averaged 33%. By indicating that SSR amplitude change is relatively specific to the agonist muscle, this finding eliminates a number of nonspecific mechanisms as possible origins of SSR amplitude change. Thus it supports the potential value of the SSR as a system for studying the neuronal and synaptic bases of memory in the primate central nervous system (CNS).


1985 ◽  
Vol 54 (2-3) ◽  
pp. 165-171 ◽  
Author(s):  
Jonathan R. Wolpaw ◽  
Julie A. O’Keefe ◽  
Victor A. Kieffer ◽  
Michael G. Sanders

1987 ◽  
Vol 57 (2) ◽  
pp. 443-459 ◽  
Author(s):  
J. R. Wolpaw

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)


1983 ◽  
Vol 267 (1) ◽  
pp. 196-200 ◽  
Author(s):  
Jonathan R. Wolpaw ◽  
Victor A. Kieffer ◽  
Richard F. Seegal ◽  
David J. Braitman ◽  
Michael G. Sanders

1984 ◽  
Vol 300 (2) ◽  
pp. 385-391 ◽  
Author(s):  
Jonathan R. Wolpaw ◽  
Patricia A. Noonan ◽  
Julie A. O'Keefe

2015 ◽  
Vol 113 (7) ◽  
pp. 2232-2241 ◽  
Author(s):  
Chadwick B. Boulay ◽  
Xiang Yang Chen ◽  
Jonathan R. Wolpaw

Sensorimotor cortex exerts both short-term and long-term control over the spinal reflex pathways that serve motor behaviors. Better understanding of this control could offer new possibilities for restoring function after central nervous system trauma or disease. We examined the impact of ongoing sensorimotor cortex (SMC) activity on the largely monosynaptic pathway of the H-reflex, the electrical analog of the spinal stretch reflex. In 41 awake adult rats, we measured soleus electromyographic (EMG) activity, the soleus H-reflex, and electrocorticographic activity over the contralateral SMC while rats were producing steady-state soleus EMG activity. Principal component analysis of electrocorticographic frequency spectra before H-reflex elicitation consistently revealed three frequency bands: μβ (5–30 Hz), low γ (γ1; 40–85 Hz), and high γ (γ2; 100–200 Hz). Ongoing (i.e., background) soleus EMG amplitude correlated negatively with μβ power and positively with γ1 power. In contrast, H-reflex size correlated positively with μβ power and negatively with γ1 power, but only when background soleus EMG amplitude was included in the linear model. These results support the hypothesis that increased SMC activation (indicated by decrease in μβ power and/or increase in γ1 power) simultaneously potentiates the H-reflex by exciting spinal motoneurons and suppresses it by decreasing the efficacy of the afferent input. They may help guide the development of new rehabilitation methods and of brain-computer interfaces that use SMC activity as a substitute for lost or impaired motor outputs.


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