Plasticity in Reflex Pathways Controlling Stepping in the Cat

1997 ◽  
Vol 78 (3) ◽  
pp. 1643-1650 ◽  
Author(s):  
P. J. Whelan ◽  
K. G. Pearson

Whelan, P. J. and K. G. Pearson. Plasticity in reflex pathways controlling stepping in the cat. J. Neurophysiol. 78: 1643–1650, 1997. Previous studies have shown that stimulation of group ‘I’ afferents from ankle extensor muscles can prolong the cycle period in decerebrate walking cats and that the magnitude of these effects can be altered after chronic axotomy of the lateral-gastrocnemius/soleus (LGS) nerve. The effectiveness of LGS group I afferents in prolonging the cycle period decreases after axotomy, whereas the effectiveness of the uncut medial-gastrocnemius (MG) group I afferents is increased. The objectives of this investigation were to establish the time course of these changes in effectiveness and to determine whether these changes persist after transection of the spinal cord. The effects of stimulating the LGS and/or MG group I afferents on the cycle period were examined in 22 walking decerebrate animals in which one LGS nerve had been cut for 2 to 31 days. The effectiveness of LGS group I afferents declined progressively in the postaxotomy period, beginning with significant decreases at 3 days and ending close to zero effectiveness at 31 days. Large increases in the effectiveness of MG group I afferents occurred 5 days after axotomy, but there was no progressive change from 5 to 31 days. To test whether these changes in effectiveness were localized to sites within the spinal cord, the cord was transected in some decerebrate animals and stepping induced by theadministration of L-DOPA L-3-4 dihydroxyphenylalanine (LDOPA) and Nialamide. The effects of stimulating the MG and/or the LGS group I afferents on the cycle period were reexamined. In all four animals tested, stimulating the axotomized LGS group I afferents had a reduced effectiveness during locomotor activity in both the decerebrate and spinal states, whereas the increased effectiveness of the MG group I afferents was retained after transection of the spinal cord in two of five animals. Different mechanisms may be responsible for the changes in strength of the LGS and MG group I afferent pathways that project onto the rhythm generating sites in the spinal cord. This possibility follows from our observations of a linear relationship between the time after axotomy and decreased effectiveness of LGS group I afferents but no significant relationship between time postaxotomy and increased effectiveness of MG group I afferents; no significant relationship between the decreased effectiveness of LGS group I afferents and the increased effectiveness of MG group I afferents; and, after spinalization, consistent (4/4 cases) preservation of decreased LGS effectiveness but frequent (3/5 cases) loss of increased MG effectiveness.

1980 ◽  
Vol 43 (6) ◽  
pp. 1631-1644 ◽  
Author(s):  
R. P. Dum ◽  
T. T. Kennedy

1. Synaptic potentials were recorded intracellularly in tibialis anterior (TA) motoneurons following stimulation of a descending brain stem pathway, the medial longitudinal fasciculus (MLF), and three segmental inputs, the homonymous and heteronymous group Ia afferents, the group I afferents from the antagonist, and the cutaneous and muscle afferents. Intracellular stimulation of the motoneurons was used to classify them, based on the properties of the innervated muscle units, into types FF, F(int), FR, and S (6, 16). 2. The sum of the monosynaptic EPSP amplitudes resulting from stimulation of homonymous and heteronymous group Ia afferents (summed group Ia EPSP) was inversely related to motoneuron size, as assessed by motoneuron input resistance, and was inversely related to motor-unit tetanic tension. Type-FF, -FR, and -S motoneurons showed significant differences in the mean amplitude of their summed group Ia EPSPs. 3. The amplitudes of disynaptic IPSPs resulting from stimulation of group I afferents in the antagonist muscle also showed an inverse relationship to motoneuron size. The observed relationships between motoneuron size and the monosynaptic group Ia EPSP amplitude or the disynaptic group I IPSP amplitude are compatible with the “size principle” of motor-unit recruitment (26). 4. The amplitudes of the monosynaptic EPSPs evoked in TA motoneurons by stimulation of the MLF were distributed rather randomly among all types of TA motoneurons. A slight tendency of larger monosynaptic EPSPs to occur in motoneurons with larger tetanic tensions was observed. 5. The polysynaptic effects from cutaneous and muscle afferents in sural and gastrocnemius-soleus nerves were frequently excitatory on type-FF motoneurons, but were primarily inhibitory on type-FR and -S motoneurons. Clearly, the polysynaptic cutaneous and muscle inputs and the monosynaptic MLF input onto TA motoneurons show a different pattern of synaptic organization than the group I inputs. 6. In general, the synaptic organization of the TA motor nucleus is similar to that of its extensor antagonist, medial gastrocnemius (MG) (2--5, 7, 8), when analogous neural circuits are compared. This parallel organization suggests a commonality of motor-control systems for both flexor and extensor muscles.


1988 ◽  
Vol 60 (5) ◽  
pp. 1678-1694 ◽  
Author(s):  
T. C. Cope ◽  
K. R. Hickman ◽  
B. R. Botterman

1. Excitatory postsynaptic potentials (EPSPs) generated in soleus motoneurons by single homonymous Ia-fibers were measured using intracellular recording and the spike-triggered averaging technique. Two groups of barbiturate-anesthetized adult cats were studied: one with the spinal cord intact and the other with the spinal cord severed at thoracic segment 13 (T13) several hours prior to recording. 2. In cord-transected cats, single homonymous Ia-fibers produced EPSPs in soleus motoneurons that were, on average, larger and faster rising relative to normal, as they are for those produced in medial gastrocnemius (MG) motoneurons (8, 12, 13, 40). Specifically, mean EPSP amplitude and rise time were, respectively, 261 +/- 22 microV and 0.65 +/- 0.05 ms for the transected group vs. 160 +/- 21 microV and 0.96 +/- 0.08 ms for the intact group. The group means for each parameter were significantly different (P less than 0.005). 3. The group difference in EPSP amplitude was largely due to a decrease in number of small EPSPs in the transected group (11% less than 100 microV compared with the normal 41%) and not due to the occurrence of unusually large ones. Ratios of the largest to smallest amplitude EPSPs produced in the same motoneuron were similarly distributed for intact and transected groups, implying that the effect of transection on EPSP size was uniform across different Ia-fiber synapses made with the same motoneuron. Mean EPSP amplitude for each transected cat (n = 5) was larger than normal, but in some cases the increase took greater than 10 h to express itself. 4. The normal tendency for EPSP rise time to decline on average with amplitude was absent in the transected group, wherein rise time was reduced to similar average values in all amplitude categories. This suggests that the decrease in rise time occurred independently of the increase in amplitude. In contrast, EPSP half-width, which tended tow ward lower than normal values [5.63 +/- 0.36 (SE) ms vs. 6.51 +/- 0.44 ms; P greater than 0.10], decreased in proportion with rise time as evidenced by the preservation of the normal relation between those parameters in transected cats. Normalizing EPSPs by motoneuron time constant (tau) reduced the group differences in rise time and half-width, suggesting that a fall in tau contributes to the abbreviation of EPSP time course. 5. The condition of the spinal cord best accounted for differences in synaptic strength between groups.(ABSTRACT TRUNCATED AT 400 WORDS)


1979 ◽  
Vol 47 (5) ◽  
pp. 1066-1073 ◽  
Author(s):  
S. Levine

Previous workers have demonstrated that hindlimb receptors can mediate some portion of the increase in VE elicited by 2,4-dinitrophenol (DNP). Liang and Hood have recently demonstrated that these hindlimb receptors communicate with the respiratory center via afferent pathways of the lumbar spinal cord. Accordingly, to determine the quantitative contribution of these hindlimb receptors to increases in VE elicited by DNP (4 mg/kg), we compared two groups of animals with respect to ventilatory, metabolic, and thermal responses elicited by this drug. Group I animals underwent complete transection of the spinal cord at the first lumbar level, whereas the spinal cord in Group II animals remained intact. Our results indicate that Group I and Group II animals did not differ with respect to increases in VE, VO2, and rectal temperature elicited by DNP. These results suggest that hindlimb receptors do not play an obligatory role in mediating increases in VE elicited by DNP. Therefore, these observations raise the possibility that multiple afferent pathways may exist for stimulation of VE by DNP.


1995 ◽  
Vol 74 (6) ◽  
pp. 2782-2787 ◽  
Author(s):  
P. J. Whelan ◽  
G. W. Hiebert ◽  
K. G. Pearson

1. This study examines whether the efficacy of polysynaptic group I excitatory pathways to extensor motoneurons are modified after axotomy of a synergistic nerve. Previously, it has been shown that stimulation of extensor nerves at group I strength can extend the stance phase and delay swing. Stimulation of the lateral gastrocnemius and soleus (LG/S) nerve prolongs stance for the duration of the stimulus train, whereas stimulation of the medial gastrocnemius (MG) nerve moderately increases stance. Our hypothesis was that after axotomy of the LG/S nerve the efficacy of the MG group I input would increase. 2. This idea was tested in 10 adult cats that had their left LG/S nerves axotomized for 3-28 days. On the experimental day the cats were decerebrated and the left (experimental) and right (control) LG/S and MG nerves were stimulated during late stance as the animals were walking on a motorized treadmill. A significant increase in the efficacy of the left MG nerve occurred 5 days after axotomy of the LG/S nerve when compared with the control response. By contrast, the previously cut LG/S nerve showed a reduction in efficacy after 3 days compared with the control limb. 3. Functionally, this plasticity may be an important mechanism by which the strength of the group I pathway is calibrated to different loads on the extensor muscles.


1983 ◽  
Vol 338 (1) ◽  
pp. 113-128 ◽  
Author(s):  
P J Harrison ◽  
E Jankowska ◽  
T Johannisson

2010 ◽  
Vol 103 (6) ◽  
pp. 3195-3204 ◽  
Author(s):  
Isaac Kurtzer ◽  
J. Andrew Pruszynski ◽  
Stephen H. Scott

Feedback control of our limbs must account for the unexpected offset of mechanical perturbations. Here we examine the evoked activity of elbow flexor and extensor muscles to torque pulses lasting 22–152 ms and how torque offset impacts activity in the long-latency (45–100 ms) and voluntary epochs (120–180 ms). For each pulse width, we found a significant attenuation of muscle activity ∼30 ms after the offset of torque compared with when the torque was sustained. The brief time between the offset of torque and the attenuation of muscle activity implicates group I afferents acting through a spinal pathway, because this route is the only one fast enough and short enough to be responsible. Moreover, elbow muscle activity in the subsequent 20–45 ms following torque-offset was ∼35% smaller than when the torque was sustained. These results show that a fast spinal process can powerfully attenuate corrective responses of the arm to a torque perturbation.


1993 ◽  
Vol 70 (3) ◽  
pp. 1009-1017 ◽  
Author(s):  
K. G. Pearson ◽  
D. F. Collins

1. Rhythmic locomotor activity was evoked in clonidine-treated acute and chronic spinal cats, and the effect of stimulating group I afferents from the plantaris muscle on the timing and magnitude of bursts in medial gastrocnemius (MG) motoneurons was examined. 2. The locomotor rhythm was entrained when group I afferents in the plantaris nerve were electrically stimulated with trains of stimuli presented at rates above and below the intrinsic frequency of the rhythmic activity. During entrainment at rates higher than the intrinsic frequency, a burst of activity in ipsilateral MG motoneurons was initiated approximately 40 ms after the onset of each stimulus train. At lower rates of entrainment the onset of MG bursts preceded the onset of the stimulus trains, and each stimulus train had an excitatory effect on the MG burst with a latency in the range of 30-50 ms. A similar excitatory effect was observed when the stimulus trains were triggered at a preset delay after the endogenous generation of the MG bursts. 3. The excitatory action of plantaris group I afferents on the MG motoneurons was only seen during periods of locomotor activity. In the absence of rhythmic activity, the same stimulus trains reduced any ongoing tonic activity in MG motoneurons. 4. Vibration of the plantaris muscle to preferentially activate group Ia afferents neither entrained the locomotor rhythm nor increased the magnitude of the MG bursts. 5. We conclude that during locomotor activity, input from group Ib afferents of the plantaris muscle has an excitatory action on the system of interneurons generating the extensor bursts, i.e., on the extensor half-center of the central rhythm generator.(ABSTRACT TRUNCATED AT 400 WORDS)


2007 ◽  
Vol 98 (5) ◽  
pp. 2525-2536 ◽  
Author(s):  
Yury P. Gerasimenko ◽  
Ronaldo M. Ichiyama ◽  
Igor A. Lavrov ◽  
Gregoire Courtine ◽  
Lance Cai ◽  
...  

We hypothesized that epidural spinal cord stimulation (ES) and quipazine (a serotonergic agonist) modulates the excitability of flexor and extensor related intraspinal neural networks in qualitatively unique, but complementary, ways to facilitate locomotion in spinal cord–injured rats. To test this hypothesis, we stimulated (40 Hz) the S1 spinal segment before and after quipazine administration (0.3 mg/kg, ip) in bipedally step-trained and nontrained, adult, complete spinal (mid-thoracic) rats. The stepping pattern of these rats was compared with control rats. At the stimulation levels used, stepping was elicited only when the hindlimbs were placed on a moving treadmill. In nontrained rats, the stepping induced by ES and quipazine administration was non–weight bearing, and the cycle period was shorter than in controls. In contrast, the stepping induced by ES and quipazine in step-trained rats was highly coordinated with clear plantar foot placement and partial weight bearing. The effect of ES and quipazine on EMG burst amplitude and duration was greater in flexor than extensor motor pools. Using fast Fourier transformation analysis of EMG bursts during ES, we observed one dominant peak at 40 Hz in the medial gastrocnemius (ankle extensor), whereas there was less of dominant spectral peak in the tibialis anterior (ankle flexor). We suggest that these frequency distributions reflect amplitude modulation of predominantly monosynaptic potentials in the extensor and predominantly polysynaptic pathways in the flexor muscle. Quipazine potentiated the amplitude of these responses. The data suggest that there are fundamental differences in the circuitry that generates flexion and extension during locomotion.


1990 ◽  
Vol 64 (4) ◽  
pp. 1303-1318 ◽  
Author(s):  
C. L. Cleland ◽  
W. Z. Rymer

1. The goal of this study was to characterize the clasp-knife reflex by the use of stretch and isometric contraction of ankle extensor and flexor muscles in decerebrated cats with bilateral dorsal hemisections of their spinal cords at segment T12. 2. Stretch of an extensor muscle evoked inhibition in both homonymous and synergistic extensor muscles. The similarities between homonymous and synergistic inhibition suggest that similar neural mechanisms were responsible. 3. Homonymous and synergistic clasp-knife inhibition showed several characteristic features: 1) inhibition was evoked only by large stretches that produced significant muscle force. Short stretches that did not produce large forces evoked only excitation; 2) the magnitude of clasp-knife inhibition increased with increasing initial motor output, as reflected in the level of rectified EMG; 3) the time course of reflex inhibition evoked by ramp-and-hold stretch was characterized by segmentation of EMG during ramp stretch, dynamic overshoot of inhibition at the end-of-ramp stretch, and slow but usually complete decay of inhibition during maintained stretch; 4) inhibition persisted beyond the termination of stretch, and 5) inhibition showed adaptation to repeated stretch. 4. Isometric contraction of the soleus or medial gastrocnemius, produced by electrical stimulation of the muscle nerve, also evoked powerful synergistic-reflex inhibition via similar mechanisms as stretch-evoked, clasp-knife inhibition. Stretch evoked a greater degree of inhibition than did contraction, indicating that receptors responsive to both stretch and contraction contribute to clasp-knife inhibition. 5. The reflex effects produced by stretching the soleus or medial gastrocnemius were not confined to the homonymous and close synergistic muscles. Extensor muscles were inhibited and flexor muscles were excited throughout the hindlimb, which paralleled the pattern of a flexion-withdrawal reflex evoked by cutaneous stimulation. 6. Stretch of a flexor muscle, the tibialis anterior, evoked the same spatial pattern and time course of reflex action as stretch of an extensor muscle--inhibition of extensor muscles and excitation of flexor muscles throughout the hindlimb, including homonymous excitation of the tibialis anterior. 7. We conclude that neither Golgi tendon organs nor secondary spindle afferents are likely to contribute significantly to clasp-knife inhibition because their responses to stretch and isometric contraction differ from the reflex actions evoked by stretch and contraction.(ABSTRACT TRUNCATED AT 400 WORDS)


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