Expansion of nociceptive withdrawal reflex receptive fields in spinal cord injured humans

OBJECTIVE: In spinal cord injured (SCI) subjects, exaggerated withdrawal reflexes associated with a dominant flexor pattern irrespective of stimulation site have been reported. In the present study, withdrawal reflex receptive field (RRF) was determined in complete SCI subjects (N=9). METHODS: Distributed electrical stimulation was applied to the sole of the foot, and reflexes in tibialis anterior, soleus, biceps femoris, and vastus lateralis muscles were recorded together with knee and ankle movement trajectories. A group of spinally intact subjects (N=10) were included as controls. With the subjects in supine position, stimulation was applied to 10 different sites on the foot sole. Based on the tibialis anterior reflex threshold for stimulation on the mid foot sole, two stimulus intensities (1.1 times the reflex threshold and 1.4 times the reflex threshold) were used for all 10 sites. RESULTS: In SCI subjects, dorsi-flexion dominated independent of stimulus site and the tibialis anterior RRF covered the entire foot sole in contrast to a well-defined tibialis anterior receptive field at the medial, distal foot sole in the spinally intact subjects. Further, the soleus RRF also covered the entire sole in the SCI subjects. The reflexes in biceps femoris and vastus lateralis muscles were small and associated with weak knee flexion at all 10 sites in the SCI subjects and in the controls. CONCLUSIONS: The RRF of the ankle flexor and the ankle extensor muscles both covered the entire sole of the foot indicating an expansion of the RRFs following spinal cord injury. The expansion is most likely due to lack of descending inhibitory control and/or increased sensitivity of the spinal reflex loop in the SCI subjects. SIGNIFICANCE: The study improves the understanding of spinal reflex control in spinal intact and spinal cord injured subjects.     

Long latency postural responses are functionally modified by cognitive set.

We examined how cognitive set influences the long latency components of normal postural responses in the legs. We disturbed the postural stability of standing human subjects with sudden toe-up ankle rotations. To influence the subjects' cognitive set, we varied the rotation amplitude either predictably (serial 4 degrees versus serial 10 degrees) or unpredictably (random mixture of 4 degrees and 10 degrees). The subjects' responses to these ankle rotations were assessed from the EMG activity of the tibialis anterior, the medial gastrocnemius, and the vastus lateralis muscles of the left leg. The results indicate that, when the rotation amplitude is predictable, only the amplitude of the long latency (LL) response in tibialis anterior and vastus lateralis varied directly with perturbation size. Furthermore, when the rotation amplitude is unpredictable, the central nervous system selects a default amplitude for the LL response in the tibialis anterior. When normal subjects are exposed to 2 perturbation amplitudes which include the potential risk of falling, the default LL response in tibialis anterior appropriately anticipates the larger amplitude perturbation rather than the smaller or an intermediate one.     

The effect of posture on the normal and pathological auditory startle reflex.

The effect of posture on the EMG pattern of the normal auditory startle reflex was investigated. The startle response to an unexpected auditory tone was studied in eleven normal subjects when standing, and in six normal subjects when sitting relaxed or tonically plantar flexing both feet. Reflex EMG activity was recorded in the tibialis anterior and soleus about twice as frequently when standing, than when sitting relaxed. In addition, the median latencies to onset of reflex EMG activity in the tibialis anterior and soleus were about 40 and 60 ms shorter during standing, than when sitting relaxed. No short latency EMG activity was recorded in the calf muscles during tonic plantar flexion of the feet, while sitting. The effect of posture on the EMG pattern of the pathological auditory startle reflex was studied in five patients with hyperekplexia. In three patients the latency to onset of reflex EMG activity in the tibialis anterior was shorter when standing, than when sitting relaxed. The EMG pattern of the reflex response to sound was studied in detail in two of these patients and consisted of up to three successive components. The expression of each EMG component depended on the postural set of the limbs. In particular, a distinct short latency component was found in posturally important muscles following auditory stimulation. This short latency component was not recorded when sitting relaxed. It is concluded that the EMG pattern of the physiological and pathological auditory startle response is not fixed, but may change with the postural stance of the body. This finding supports the theory that the normal startle reflex and the abnormal startle reflex in hyperekplexia have a common brainstem origin.     

Gradual enlargement of human withdrawal reflex receptive fields following repetitive painful stimulation

Dynamic changes in the topography of the human withdrawal reflex receptive fields (RRF) were assessed by repetitive painful stimuli in 15 healthy subjects. A train of five electrical stimuli was delivered at a frequency of 3 Hz (total train duration 1.33 s). The train was delivered in random order to 10 electrode sites on the sole of the foot. Reflexes were recorded from tibialis anterior, soleus, vastus lateralis, biceps femoris, and iliopsoas (IL). The RRF changes during the stimulus train were assessed during standing with even support on both legs and while seated. The degree of temporal summation was depending on stimulation site. At the most sensitive part of the RRF, a statistically significant increase in reflex size was seen after two stimuli while four stimuli were needed to observe reflex facilitation at less sensitive electrode sites. Hence, the region from which reflexes could be evoked using the same stimulus intensity became larger through the train, that is, the RRF was gradually expanding. Reflexes evoked by stimuli four and five were of the same size. No reflex facilitation was seen at other stimulus sites outside the RRF. In all muscles except in IL, the largest reflexes were evoked when the subjects were standing. In the ankle joint, the main withdrawal pattern consisted of plantar flexion and inversion when the subjects were standing while dorsi-flexion was prevalent in the sitting position. Up to 35 degrees of knee and hip flexion were evoked often leading to a lift of the foot from the floor during standing. In conclusion, a gradual expansion of the RRF was seen in all muscles during the stimulus train. Furthermore, the motor programme task controls the reflex sensitivity within the reflex receptive field and, hence, the sensitivity of the temporal summation mechanism.     

Modular organization of human leg withdrawal reflexes elicited by electrical stimulation of the foot sole.

Human withdrawal reflex receptive fields were determined for leg muscles by randomized, electrical stimulation at 16 different positions on the foot sole. Tibialis anterior, gastrocnemius medialis, peroneus longus, soleus, rectus femoris, and biceps femoris reflexes, and ankle joint angle changes were recorded from 14 subjects in sitting position. Tibialis anterior reflexes were evoked at the medial, distal foot and correlated well with ankle dorsal flexion. Gastrocnemius medialis reflexes were evoked on the heel and correlated with plantar flexion. Stimulation on the distal, medial sole resulted in inversion (correlated best with tibialis anterior activity), whereas stimulation of the distal, lateral sole evoked eversion. Biceps femoris reflexes were evoked on the entire sole followed by a small reflex in rectus femoris. A detailed withdrawal reflex organization, in which each lower leg muscle has its own receptive field, may explain the ankle joint responses. The thigh activity consisted primarily of flexor activation.     

Modular organization of excitatory and inhibitory reflex receptive fields elicited by electrical stimulation of the foot sole in man.

OBJECTIVES: The present study aimed to investigate how the inhibitory and excitatory reflex components of the human (polysynaptic) withdrawal reflex are organized depending on the stimulation site. The reflexes were elicited during a voluntary pre-contraction (between 10 and 20% of maximum voluntary contraction) of two antagonistic muscles. METHODS: Inhibitory and excitatory reflex receptive fields to tibialis anterior (TA) and soleus (SO) were mapped in 14 healthy subjects using randomized electrical stimulation at 16 sites of the foot sole. Low, non-painful (3x perception threshold), and high, painful (1.5x pain threshold), stimulus intensities were used. RESULTS: The inhibitory reflex receptive fields were organized in a highly functional manner supporting the action of the excitatory reflex. Together the two reflexes result in an optimal withdrawal from the stimulus. Low stimulation intensity was found sufficient to elicit the inhibitory reflex. High stimulation intensity caused a reversal of the inhibition to excitation in tibialis anterior. In soleus the inhibition was facilitated for stronger intensities. CONCLUSION: In conclusion, findings in animals of a modular organization of inhibitory reflexes are reproduced in humans.     

The H-reflex in the passive human soleus muscle is modulated faster than predicted from post-activation depression

The purpose of the present study was to investigate the influence of afferent activity (mainly homonymous Ia-afferent activity) on the modulation (post-activation depression) of the soleus H-reflex during isolated and passive sinusoidal ankle joint rotations at a speed and amplitude comparable to slow walking. The H-reflex modulation was measured in the relaxed soleus muscle on human subjects during different imposed patterns of 20° haversine ankle joint rotations (0.5–0.6 Hz) while they were sitting comfortably in a chair. Eighteen healthy males and four male patients with clinically complete spinal cord lesion above the soleus motoneuron pool participated in the study. During a single dorsi–plantar flexion rotation the H-reflex was depressed to 27±7% (mean±S.E.M.) of the initial level within 600 ms. The course of this depression was reversed when the dorsi-flexion velocity started to decrease. At the end of the dorsi-flexion movement the depression was already relieved to a level of 73±6% of the initial level. The H-reflex returned more slowly to the initial level within 2 s after the end of the movement cycle. During two consecutive ankle joint rotations and continuous ankle joint rotations both at 0.5 Hz the H-reflex was modulated but also generally depressed while the movement was imposed. The reflex only returned to the reference level after the movements were stopped. These observations indicate the action of a fast and a slow mechanism in the post-activation depression of the soleus H-reflex. The H-reflex modulations observed in the spinal cord injured patients were comparable to the reflex modulations observed in the healthy subjects, except the depressions were smaller. This suggests that a major part of the amplitude of the H-reflex modulation observed in healthy subjects was caused by peripheral and spinal influences. The fast 500 ms recovery of the H-reflex had a time course comparable to presynaptic inhibition. The slow 2 s recovery after the end of a given imposed movement may be explained by a change in the probability of transmitter release from the homonymous soleus Ia-afferent synaptic terminals after repeated activations.     

The action of plantar pressure on flexion reflex pathways in the isolated human spinal cord.

OBJECTIVE: To investigate the conditioning effects of plantar pressure on flexion reflex excitability in patients with motor complete spinal cord injury (SCI). METHODS: In five motor complete SCI subjects, the non-nociceptive flexion reflex was evoked via electrical stimulation of the right sural nerve and was recorded from the ipsilateral tibialis anterior muscle. Pressure ranging from 25 to 80kPa was applied to the metatarsal heads through an adjustable platform incorporated into a foot rest and a comparison of the reflex size made between control conditions and during pressure application. RESULTS: In all subjects, a significant depression of the long latency flexion reflex was observed when pressure was applied to the foot sole. The short latency flexion reflex appearing at latencies less than 100ms was absent in all patients. CONCLUSIONS: The results demonstrate that flexion reflex excitability in the isolated human spinal cord can be modulated by adequate activation of plantar mechanoreceptors. SIGNIFICANCE: Activation of plantar mechanoreceptors is a feature of normal standing and walking. Rehabilitation for standing and walking in SCI commonly uses body weight support based protocols. The strong inhibitory actions of plantar pressure on reflex pathways in the isolated human spinal cord suggest that sensory feedback from the foot sole may be an important factor in successful rehabilitation of standing and stepping in SCI patients.     

Relative changes with contraction in the central excitability state of the tibialis anterior and calf muscles.

F responses were recorded from the surface of the tibialis muscle and medial aspect of the soleus muscle in 14 normal subjects. The persistence (that is the fraction of measurable F responses found with a series of supramaximal stimuli) and average F amplitudes (measured peak-to-peak and based on at least five F responses) were determined both at rest and with isometric contraction with the ankle maintained at 90 degrees. Although the persistence at rest was significantly less in the tibialis anterior soleus than the (p less than 0.001), no significant difference was found with the muscles contracted. This was associated with a significant increase in both average F amplitudes and average F amplitude/direct motor response ratios in the tibialis anterior in comparison to the soleus. In four of the subjects, studies were also performed when the H reflex in the soleus muscle was eliminated by thigh compression. Comparable changes in both F response persistence and average F amplitude were found with and without an H reflex. These data indicate that, in contrast to the situation at rest, with isometric contraction the "central excitatory state" of the tibialis anterior is at least as great as in its antagonist antigravity muscles and that this is not due simply to increased large fiber reflex input associated with agonist contraction.     

Tibialis Anterior and Soleus Withdrawal Reflexes Elicited by Electrical Stimulation of the Sole of the Foot during Gait

The aim of the present study was to investigate the modulation and functional importance of nociceptive withdrawal reflexes elicited from the sole of the foot and recorded from the soleus (SOL) and tibialis anterior (TA) muscles during gait. Cutaneous electrical stimulation delivered at four locations of the sole of the foot was used to elicit the withdrawal reflex. Reflexes were recorded from eight healthy subjects during treadmill walking. The reflexes were elicited at heel‐contact, during foot‐flat, at heel‐off, and during mid‐swing. The reflexes evoked in TA were largest when the arch of the foot was stimulated, and smallest following stimulation of the heel (significant difference during stance, p ≤ 0.002). The largest soleus responses were elicited when the arch of the foot was stimulated (significant difference compared with the fifth metatarsophalangeal joint, stimulation after heel‐contact, p < 0.05). The TA reflex, expressed as a proportion of the electromyogram during unperturbed gait, was smallest during swing (p < 0.05, compared with stance) whereas the SOL reflex was maximal during swing (p < 0.05, compared with stance). The results suggest that the modulation of the reflex promotes an appropriate withdrawal while preserving balance and continuity of motion. These results may have applications in assisting gait of hemiplegics.