Effect of acute lateral hemisection of the spinal cord on spinal neurons of postural networks (original) (raw)
Related papers
Effects of acute spinalization on neurons of postural networks
Scientific Reports, 2016
Postural limb reflexes (PLRs) represent a substantial component of postural corrections. Spinalization results in loss of postural functions, including disappearance of PLRs. The aim of the present study was to characterize the effects of acute spinalization on two populations of spinal neurons (F and E) mediating PLRs, which we characterized previously. For this purpose, in decerebrate rabbits spinalized at T12, responses of interneurons from L5 to stimulation causing PLRs before spinalization, were recorded. The results were compared to control data obtained in our previous study. We found that spinalization affected the distribution of F-and E-neurons across the spinal grey matter, caused a significant decrease in their activity, as well as disturbances in processing of posture-related sensory inputs. A twofold decrease in the proportion of F-neurons in the intermediate grey matter was observed. Location of populations of F-and E-neurons exhibiting significant decrease in their activity was determined. A dramatic decrease of the efficacy of sensory input from the ipsilateral limb to F-neurons, and from the contralateral limb to E-neurons was found. These changes in operation of postural networks underlie the loss of postural control after spinalization, and represent a starting point for the development of spasticity. In quadrupeds, deviations of the trunk from the dorsal-side-up orientation cause postural corrections, which are generated mainly on the basis of signals from limb mechanoreceptors 1-3. Earlier, we studied postural limb reflexes (PLRs) in decerebrate rabbits. We have found that the spinal cord contains neuronal networks generating spinal PLRs; however, their efficacy is low, and supraspinal influences substantially contribute to generation of PLRs 4,5. Recently, populations of spinal interneurons contributing to generation of PLRs have been characterized 6. It was suggested that PLRs in intact animals substantially contribute to postural corrections 3,4. Spinalization abolishes postural functions in quadrupeds, and postural control in spinal animals (including PLRs) does not recover with time 7-10. After spinalization, spasticity (manifested in postural function as incorrect motor responses to posture-related sensory signals) gradually develops, suggesting plastic changes in the spinal postural networks 10. An immediate reaction to spinalization is "spinal shock", characterized by a dramatic reduction of extensor tone and most spinal reflexes including PLRs 10-13. The main reason for spinal shock is a loss of supraspinal influences on spinal networks 13,14. It was demonstrated that one of the factors responsible for the reduced efficacy of spinal reflexes after spinalization is a decrease in the excitability of spinal motoneurons 15-17. Recently, by using the method of "reversible spinalization" (a temporal cold block of signal transmission in spinal pathways) we have demonstrated that another factor is a decrease in the activity of most spinal interneurons, including PLR-related neurons 14. However, the method of reversible spinalization did not allow for characterizing in detail the spinal postural networks at the acute stage of spinalization since the state of functional spinalization was maintained only for a few minutes (to prevent damage of the nervous tissue by cooling). The overall goal of our current research is to reveal the changes in spinal postural networks that may underlie the development of spasticity 18. The aim of the present study was to characterize in detail the starting point for these changes, that is the state of the spinal postural networks at the acute stage of spinalization. For this purpose, the responses of interneurons from L5 to stimulation that evoked PLRs before spinalization were recorded in decerebrate rabbits spinalized at T12. The results were compared with control data obtained in our previous study 6. A brief account of this study has been published in abstract form 19. Results Effect of spinalization on PLRs. Before spinalization, in all preparations, the whole platform tilts (Fig. 1c) evoked PLRs similar to those described in detail in our earlier studies 4,20. They included activation of extensors
Impairment and Recovery of Postural Control in Rabbits With Spinal Cord Lesions
Journal of Neurophysiology, 2005
The aim of this study was to characterize impairment and subsequent recovery of postural control after spinal cord injuries. Experiments were carried out on rabbits with three types of lesion—a dorsal (D), lateral (L), or ventral (V) hemisection (HS) at T12 level. The animals were maintaining equilibrium on a platform periodically tilted in the frontal plane. We assessed the postural limb/trunk configuration from video recordings and postural reflexes in the hindquarters from kinematical and electromyographic (EMG) recordings. We found that for a few days after DHS or LHS, the animals were not able to maintain the dorsal-side-up position of their hindquarters. This ability was then gradually restored, and the dynamic postural reflexes reached the prelesion value within 2–3 wk. By contrast, a VHS almost completely abolished postural reflexes, and they did not recover for ≥7 wk. The DHS, LHS, and VHS caused immediate and slowly compensated changes in the postural limb/trunk configurat...
Effects of Reversible Spinalization on Individual Spinal Neurons
Journal of Neuroscience, 2013
Postural limb reflexes (PLRs) represent a substantial component of the postural system responsible for stabilization of dorsal-side-up trunk orientation in quadrupeds. Spinalization causes spinal shock, that is a dramatic reduction of extensor tone and spinal reflexes, including PLRs. The goal of our study was to determine changes in activity of spinal interneurons, in particular those mediating PLRs, that is caused by spinalization. For this purpose, in decerebrate rabbits, activity of individual interneurons from L5 was recorded during stimulation causing PLRs under two conditions: (1) when neurons received supraspinal influences and (2) when these influences were temporarily abolished by a cold block of spike propagation in spinal pathways at T12 ("reversible spinalization"; RS). The effect of RS, that is a dramatic reduction of PLRs, was similar to the effect of surgical spinalization. In the examined population of interneurons (n ϭ 199), activity of 84% of them correlated with PLRs, suggesting that they contribute to PLR generation. RS affected differently individual neurons: the mean frequency decreased in 67% of neurons, increased in 15%, and did not change in 18%. Neurons with different RS effects were differently distributed across the spinal cord: 80% of inactivated neurons were located in the intermediate area and ventral horn, whereas 50% of nonaffected neurons were located in the dorsal horn. We found a group of neurons that were coactivated with extensors during PLRs before RS and exhibited a dramatic (Ͼ80%) decrease in their activity during RS. We suggest that these neurons are responsible for reduction of extensor tone and postural reflexes during spinal shock.
Changes in Activity of Spinal Postural Networks at Different Time Points After Spinalization
Frontiers in Cellular Neuroscience, 2019
Postural limb reflexes (PLRs) are an essential component of postural corrections. Spinalization leads to disappearance of postural functions (including PLRs). After spinalization, spastic, incorrectly phased motor responses to postural perturbations containing oscillatory EMG bursting gradually develop, suggesting plastic changes in the spinal postural networks. Here, to reveal these plastic changes, rabbits at 3, 7, and 30 days after spinalization at T12 were decerebrated, and responses of spinal interneurons from L5 along with hindlimb muscles EMG responses to postural sensory stimuli, causing PLRs in subjects with intact spinal cord (control), were characterized. Like in control and after acute spinalization, at each of three studied time points after spinalization, neurons responding to postural sensory stimuli were found. Proportion of such neurons during 1st month after spinalization did not reach the control level, and was similar to that observed after acute spinalization. In contrast, their activity (which was significantly decreased after acute spinalization) reached the control value at 3 days after spinalization and remained close to this level during the following month. However, the processing of postural sensory signals, which was severely distorted after acute spinalization, did not recover by 30 days after injury. In addition, we found a significant enhancement of the oscillatory activity in a proportion of the examined neurons, which could contribute to generation of oscillatory EMG bursting. Motor responses to postural stimuli (which were almost absent after acute spinalization) reappeared at 3 days after spinalization, although they were very weak, irregular, and a half of them was incorrectly phased in relation to postural stimuli. Proportion of correct and incorrect motor responses remained almost the same during the following month, but their amplitude gradually increased. Thus, spinalization triggers two processes of plastic changes in the spinal postural networks: rapid (taking days) restoration of normal activity level in spinal interneurons, and slow (taking months) recovery of motoneuronal excitability. Most likely, recovery of interneuronal activity underlies reappearance of motor responses to postural stimuli. However, absence of recovery of normal processing of postural sensory signals and enhancement of oscillatory activity of neurons result in abnormal PLRs and loss of postural functions.
2010
Edgerton. Plasticity of spinal cord reflexes after a complete transection in adult rats: relationship to stepping ability. . Changes in epidurally induced (S1) spinal cord reflexes were studied as a function of the level of restoration of stepping ability after spinal cord transection (ST). Three types of responses were observed. The early response (ER) had a latency of 2.5 to 3 ms and resulted from direct stimulation of motor fibers or motoneurons. The middle response (MR) had a latency of 5 to 7 ms and was monosynaptic. The late response (LR) had a latency of 9 to 11 ms and was polysynaptic. After a complete midthoracic ST, the LR was abolished, whereas the MR was facilitated and progressively increased. The LR reappeared about 3 wk after ST and increased during the following weeks. Restoration of stepping induced by epidural stimulation at 40 Hz coincided with changes in the LR. During the first 2 wk post-ST, rats were unable to step and electrophysiological assessment failed to show any LR. Three weeks post-ST, epidural stimulation resulted in a few steps and these coincided with reappearance of the LR. The ability of rats to step progressively improved from wk 3 to wk 6 post-ST. There was a continuously improved modulation of rhythmic EMG bursts that was correlated with restoration of the LR. These results suggest that restoration of polysynaptic spinal cord reflexes after complete ST coincides with restoration of stepping function when facilitated by epidural stimulation. Combined, these findings support the view that restoration of polysynaptic spinal cord reflexes induced epidurally may provide a measure of functional restoration of spinal cord locomotor networks after ST.
Plasticity in the descending motor pathways after spinal cord hemisection
International Congress Series, 2005
The present study evaluates the motor functional recovery after C2 spinal cord hemisection combined with contralateral brachial root transection, which causes a condition that is similar to the crossed phrenic phenomenon (CPP). Descending motor pathways, including the reticulospinal extrapyramidal tract and corticospinal pyramidal tracts, were evaluated by transcranial magnetic motor-evoked potentials (mMEPs) and direct cortical electrical motor-evoked potentials (eMEP), respectively. All MEPs recorded from the left forelimb were abolished immediately after the left C2 hemisection. Left mMEPs recovered dramatically immediately after contralateral right brachial root transection. Corticospinal eMEPs never recovered, regardless of transection. The facilitation of mMEPs in animals that had undergone combined contralateral root transection was well correlated with open-field behavioral motor performance. D
Kinematic Analysis of Locomotory Recovery following Dorsal Hemisection of Spinal Cord in the Rat
Spinal Surgery, 1999
Using computerized motion analysis techniques, kinematics of foot trajectories were quantitatively analyzed in twelve rats befOre and after dorsal spinal cord hemisection at T6 level. Although overground locomotion in these animals returned to normal within fbur weeks, somc kinematic variables during treadmill locomotion did not recover to pre-lesion levels. Immediately following dorsal hernisection, amplitudes of both hindfeet horizontal and vertical movements were dramatically reduced. Howcver, in three weeks, the amplitudcs of horizontal movement (stride length) bccame significantly larger than that of pre-!csion strides. On the other hand, amplitude of hindlimb vertical movement showed very liule recovery. Forelimb-hindlimb coordination was also disrupted initially but returned to normal within three weeks, The duration of hindlimb swing phase became significantly longer after section and gradually recovercd, but never to prelesion levels. Interesting]y, arnplitudes of forelimb venical movement, which was depressed initially, became significantly larger three weeks after lesion. A dramatic increase in the statistical variation of limb kinematics, which persisted even after motor recovery, is an irnportant parameter for the evaluation of neural deficits in spinal cord iajuries. Kinematic analysis using computerizecl motion analysis techniques is a sensitive technique fOr the detection of minor motor deficits following ncrve iniures.
Brain Research, 2006
We have investigated the motor changes in rats subjected to a moderate photochemical injury on mid-thoracic (T8) or high lumbar (L2) spinal cord segments. Fourteen days after surgery, L2 injured animals presented gross locomotor deficits (scored 10 ± 2.8 in the BBB scale), decreased amplitude of motor-evoked potentials (MEPs) recorded on tibialis anterior (TA) and plantar (PL) muscles (24% and 6% of the preoperative mean values, respectively), reduced M wave amplitudes (75%, 62%), and also facilitated monosynaptic reflexes evidenced by an increase of the H/M amplitude ratio (158% and 563%). On the other hand, T8 injured animals had only slight deficits in locomotion (18 ± 0.6 in the BBB scale), a minimal reduction in MEP amplitudes (78% and 71% in TA and PL muscles), normal M wave amplitudes, and a milder increase of the H/M ratio in the TA muscle (191%) but less pronounced in the PL muscle (172%). The percentage of spared tissue at the site of injury was similar in both experimental groups (L2: 79% and T8: 82%). Taken together, these results indicate that lumbar spinal injuries have more severe consequences on hindlimb motor output than injuries exerted on thoracic segments. The causes of this anatomical difference may be attributed to damage inflicted on the central pattern generator of locomotion resulting in dysfunction of lumbar motoneurons and altered spinal reflexes modulation.
Journal of Neurophysiology, 2009
Frigon A, Barrière G, Leblond H, Rossignol S. Asymmetric changes in cutaneous reflexes after a partial spinal lesion and retention following spinalization during locomotion in the cat. involves dynamic interactions between the spinal cord, supraspinal signals, and peripheral sensory inputs. After incomplete spinal cord injury (SCI), interactions are disrupted, and remnant structures must optimize function to maximize locomotion. We investigated if cutaneous reflexes are altered following a unilateral partial spinal lesion and whether changes are retained within spinal circuits after complete spinal transection (i.e., spinalization). Four cats were chronically implanted with recording and stimulating electrodes. Cutaneous reflexes were evoked with cuff electrodes placed around left and right superficial peroneal nerves. Control data, consisting of hindlimb kinematics and electromyography (bursts of muscular activity and cutaneous reflexes), were recorded during treadmill locomotion. After stable control data were achieved (53-67 days), a partial spinal lesion was made at the 10th or 11th thoracic segment (T 10 -T 11 ) on the left side. Cats were trained to walk after the partial lesion, and following a recovery period (64 -80 days), a spinalization was made at T 13 . After the partial lesion, changes in short-latency excitatory (P1) homologous responses between hindlimbs, evoked during swing, were largely asymmetric in direction relative to control values, whereas changes in longer-latency excitatory (P2) and crossed responses were largely symmetric in direction. After spinalization, cats could display hindlimb locomotion within 1 day. Early after spinalization, reflex changes persisted a few days, but over time homologous P1 responses increased symmetrically toward or above control levels. Therefore changes in cutaneous reflexes after the partial lesion and retention following spinalization indicate an important spinal plasticity after incomplete SCI.
Plasticity of the Spinal Neural Circuitry After Injury*
Annual Review of Neuroscience, 2004
Motor function is severely disrupted following spinal cord injury (SCI). The spinal circuitry, however, exhibits a great degree of automaticity and plasticity after an injury. Automaticity implies that the spinal circuits have some capacity to perform complex motor tasks following the disruption of supraspinal input, and evidence for plasticity suggests that biochemical changes at the cellular level in the spinal cord can be induced in an activity-dependent manner that correlates with sensorimotor recovery. These characteristics should be strongly considered as advantageous in developing therapeutic strategies to assist in the recovery of locomotor function following SCI. Rehabilitative efforts combining locomotor training pharmacological means and/or spinal cord electrical stimulation paradigms will most likely result in more effective methods of recovery than using only one intervention. * Abbreviations: 5-hydroxytryptamine (5-HT); 2-amino-5-phosphonovaleric acid (AP-5); American Spinal Injury Association (ASIA); brain-derived neurotrophic factor (BDNF); central nervous system (CNS); central pattern generation (CPG); electrical stimulation (ES); electromyography (EMG); extensor digitorum longus (EDL); gamma-aminobutyric acid (GABA); glial fibrillary acidic protein (GFAP); glutamic acid decarboxylase (GAD); long-term potentiation (LTP); long-term depression (LTD); m-chlorophenylpiperazine (m-CPP); medial gastrocnemius (MG); neurotrophin-3 (NT-3); noradrenaline (NA); N-methyl-D-aspartate (NMDA); paw contact (PC); peripheral nervous system (PNS); soleus (SOL); spinal cord injury (SCI); swing-phase force field (SWPFF); tibialis anterior (TA).