The flow and disintegration of sensory information in the spinal circuitry

Bashor (1998) created a large-scale biological neural network model and used it to study the dynamic interactions in neuron populations. We adapted the model to control a single-joint musculoskeletal model during a postural task (Stienen et al., 2007). The biological neural network controls the motoneuron firing rate by combining the tonic descending excitation and the muscle spindle and Golgi tendon organ proprioceptor signals. The network with a total of 2298 neurons consists of motoneurons and several types of interneurons in six antagonistic population pairs: the motoneurons (169 neurons per pair-half) directly drive the muscles; the interneurons (five types, 196 neurons per pair-half) are exciting or inhibiting---and possibly recurrent or reciprocal---intermediates for passing the Ia (muscle length and velocity), Ib (muscle force) and II afferent (muscle length) information received from the proprioceptors on to the motoneurons. The model parameters are based on spinal recordings in cats, which are assumed to be functionally comparable with humans. With this model we showed that the model mimics the findings of human postural experiments using presynaptic inhibition of the Ia-afferents to modulate the feedback gains, with both human and model able to achieve negative feedback gains. In a pathological example, disabling one specific interneural connection simulates the experimental results in complex regional pain syndrome patients. We have further investigated the flow of sensory information in the spinal circuitry. Two aspects seem to dominate the outcome: the number of synapses the information crosses and the total stimulation effect of all inhibitory and excitatory connections. The proprioceptive feedback reaches the motoneurons directly or via one or more intermediating interneurons. The number of synaptic connections classifies these paths. For instance, for the monosynaptic stretch reflex the spinal information crosses only one synapse between muscle spindle and motoneuron. Paths that cross two or three synapses between sensor and motoneurons are called di- and trisynaptic. The influence decreases with the number of synapses due to information dilution. We found that paths that cross more than three synapses can be ignored. Paths can provide positive or negative stimulation to the motoneurons. Crossing one reciprocal or one inhibitory synapse will make the stimulus negative; crossing another makes the stimulus positive again. The total stimulation effect of the path on the motoneuron can be calculated. Note that positive stimulation results in a negative feedback path with positive gain components in feedback control diagrams. With a modeling study we investigated the effect of the sensorimotor interaction on the phase-frequency relationship of the CMC. The model includes two systems, representing the efferent and afferent pathways modeled as gains and realistic neural time delays. We found that the closed-loop formed by the sensorimotor interaction has a huge effect on the phase-frequency relationship, depending on the relative strength of the afferent pathways. Within the beta band the slope of the phase-frequency relation is reduced (i.e. is less negative than expected for a pure efferent pathway) and has a nonzero intersect. If the afferent pathways are stronger than the efferent pathways a phase advance will result, i.e. the slope can become positive. In conclusion, the phase-frequency relation emerges from the interaction in the sensorimotor loop and here we demonstrated how the relation depends on a complex interaction between the afferent and efferent pathways

Balance task and head orientation dependency of vestibular reflexes in neck muscles

Human upright posture of both the head and body is facilitated by the CNS’s ability to integrate multiple sensory feedback signals, as well as its discernibility of the motor commands that maintain this stabilization. The vestibular organ in particular detects motion of the head-in-space, which is transformed according to on-going head and body orientation into appropriate motor responses. However, when motor commands do not contribute to the control of standing posture, and are incongruent with their expected sensory consequences, vestibulomuscular responses in the lower limb undergo unconscious suppression. In this study, we investigated whether vestibular response suppression occurs in neck muscles under conditions where the muscles are active but not engaged in a task to balance the head. In addition, we examined the effects of head orientation to identify spatial transformation of vestibular reflex responses. Eight subjects were exposed to stochastic vestibular stimulation (0-75 Hz) in a seated condition while their head was either free or fixed, and rotated at either 0 or 60°. In head-free conditions, subjects were asked to rotate their head 60° to the left in order to activate agonist neck muscle pairs (sternocleidomastoid - SCM and splenius capitis - SPL). In head-fixed conditions, subjects performed isometric neck muscle contractions in yaw at orientations of 0° and 60°, as well as flexion, extension and co-contraction at an orientation of 0°. Intramuscular EMG was collected bilaterally in SCM and SPL muscles. Muscle responses correlated to the input stimuli were significant (P < 0.05) for all conditions provided the muscle was used in contraction. Neither muscle underwent the expected vestibulomuscular suppression when not engaged in the balance task (i.e. head-fixed). Nevertheless, the magnitude of the SPL responses decreased by 22% when the head was fixed whereas SCM responses were unaffected. The effect of head fixation only in SPL suggests differences in neural pathways across muscles, possibly via alternative pathways known to exist in the SPL from the well-established monosynaptic vestibulospinal inputs in SCM and SPL. For both muscles, the effect of orientation and force direction had no effect on muscles responses. Since the stimulation is fixed relative to the head, the same muscles are activated to respond to the input stimulus at both orientations and all force directions. These results indicate that the vestibular pathways connecting neck muscles are less susceptible to suppression than lower limb muscles, most likely because the monosynaptic inputs innervating them are subject to less central control

Reproducability of corticomuscular coherence:A comparison between static and perturbed tasks

Corticomuscular coherence (CMC) is used to quantify functional corticomuscular coupling during a static motor task. Although the reproducibility of CMC characteristics such as peak strength and frequency within one session is good, reproducibility of CMC between sessions is limited (Pohja et al. 2005, NeuroImage). Reproducible CMC characteristics are required in order to assess changes in corticomuscular coupling in a longitudinal study design, for example during rehabilitation. We recently demonstrated that the presence of CMC in the population in substantially increased when position perturbations are applied during an isotonic force task. Here, we assessed the reproducibility of perturbed CMC compared to unperturbed CMC. Subjects (n=10) performed isotonic wrist flexion contractions against the handle of a wrist manipulator (WM) while EEG (64 channels) and EMG of the m.flexor carpi radialis were recorded in two experimental sessions separated by at least one week. The handle of the WM either kept a neutral angle (baseline task) or imposed a small angle perturbation (perturbed task). In the baseline task, 3 subjects had significant CMC in both the first and the second sessions. In the other 7 subjects no significant CMC was found in both sessions. Between sessions, significant CMC was always found in overlapping frequency bands and generally on overlapping electrodes. In the subjects with CMC a significant cross correlation coefficient between the spectra in the two sessions was present (mean 0.57; 0.3 - 0.79). In the perturbed task CMC was present in 8 subjects in both sessions and absent in 1 subject in the two sessions. One subject had CMC only in the second session. For the subjects with CMC, the correlation coefficient between the spectra of the two sessions was significantly larger than zero with a mean of 0.68 (range 0.38 - 0.88). The presence and absence of CMC within subjects could be reproduced very well between the sessions. This was also demonstrated by the significant correlation between the spectra in the two sessions ; the degree of correlation was variable over subjects both in the baseline and the perturbed task. The reproducibility characteristics of CMC in a perturbed task are comparable or slightly better with respect to an unperturbed task. However, comparison is limited by the small number of subjects with CMC in the baseline task. Perturbed CMC is present in more subjects, which is crucial when developing methods to track corticomuscular coupling over multiple sessions, for example during rehalibitation.handles MIMO systems, and can deal with short measurement time

Vestibular contributions to lateral stabilization are bilaterally dependent during split belt walking

Vestibular information is critical for maintaining balance during locomotion, and is known to be attenuated with increasing locomotor velocity and cadence. This attenuation is muscle and phase dependent, and is thought to reflect the functional contribution of each muscle to balance control during each stride of the gait cycle. Bilaterally, the vestibular coupling is mirrored relative to the gait cycle as each leg undergoes similar modulation with variation in phase, velocity and cadence. Here, we asked whether the modulation of the vestibular contribution to each limb is bilaterally dependent. By using a split-belt treadmill with asymmetric belt speeds, we can control the locomotion properties of each leg and compare the vestibular modulation to symmetric conditions. We hypothesized that bilaterally symmetric vestibular modulation would indicate leg independent vestibular influence while bilaterally asymmetric vestibular modulation would indicate leg dependent vestibular influence. Subjects were exposed to binaural bipolar stochastic vestibular stimulation (0-25 Hz) during symmetric and asymmetric walking conditions. Symmetric trials were performed at belt speeds of 0.4 and 0.8 m/s and for 10 min. The asymmetric trial was performed at belt speeds of 0.4 and 0.8 m/s for 16 min. Subjects walked with a cadence of 78 steps/min which was easily maintained in both limbs. EMG of the bilateral medial gastrocnemii and three-dimensional ground reaction force and torques were collected. Only the last 340 strides (~ 9 min of data) were used in the analysis to avoid the adaptation that typically occurs within the first 250 strides (~ 6 min) of asymmetric walking. Significant muscle activity and lateral ground reaction forces (P < 0.01) were correlated to the input stimuli in all trials. Stimulus-EMG and -lateral ground reaction force correlations decreased at higher belt speeds during symmetric walking, as previously reported. During the split belt condition, the magnitude of correlations stimulus-EMG and -force were bilaterally asymmetric and different from their symmetric counterparts. During the asymmetric condition correlations decreased for the slow leg, but more closely resembled the responses observed during slow symmetric walking, and increased for the fast leg, but more closely resembled the responses observed during fast symmetric walking. These results indicate that the modulation of vestibular reflexes is dependent upon the specific kinematics of each leg but bilaterally linked to respond to the properties of the locomotion pattern

Time variant system identification of human limb dynamics using wavelets

The dynamic behavior (i.e. admittance) of a human limb results from the interaction between limb inertia, muscles and the central nervous system. System identification techniques assess the dynamic behavior of a limb by analyzing the limb’s response to certain perturbations. Most identification techniques require the system to behave linear and time invariant, i.e. the system’s response to the perturbation must remain unchanged during observation. However it is known that neuromuscular properties change for example with fatigue. Furthermore it has been found that the strength of afferent feedback (e.g. from muscle spindles and Golgi tendon organs) adapts to conditions like task instruction and mechanical load. So far, research mainly focused on the the steady state behavior after the system had been adapted but not on the adaptation process itself. In this study we developed a closed-loop time-variant identification technique based on wavelet cross spectra to continuously identify the admittance, i.e. the dynamic relation between input force (or torque) and the output displacement. This identification technique allowed for measurement of the human joint dynamics as a function of time while the human interacts with a mechanical load. As a second step the afferent feedback strengths were quantified by fitting a neuromuscular control model onto the admittance for each time instant. The model fit produced physiological relevant parameters, like muscle visco-elasticity resulting from (co-)contraction, afferent feedback from muscle spindles and Golgi tendon organs including neural time delays. Simulations demonstrated that the developed method is able to track time-variant behavior. Preliminary results of experimental data showed that human subjects adapt their admittance to an instantaneous change of a viscous load. In particular, the gain of the afferent feedback changed within seconds. The estimated dynamic behavior of the human joint before and after the change of the viscous load resembled the behavior as identified using traditional time-invariant techniques in two separate experiments with constant viscous loads. However, the accuracy of the estimated adaptation time of the system is yet to be determined as the method in its current form is less able to track fast changes in system behavior. Further research into time-variant closed-loop identification is recommended to improve the temporal accuracy

Stretch Evoked Potentials in Healthy Subjects and After Stroke: A Potential Measure for Proprioceptive Sensorimotor Function

Sensory feedback is of vital importance in motor control, yet rarely assessed in diseases with impaired motor function like stroke. Muscle stretch evoked potentials (StrEPs) may serve as a measure of cortical sensorimotor activation in response to proprioceptive input. The aim of this study is: 1) to determine early and late features of the StrEP and 2) to explore whether StrEP waveform and features can be measured after stroke. Consistency of StrEP waveforms and features was evaluated in 22 normal subjects. StrEP features and similarity between hemispheres were evaluated in eight subacute stroke subjects. StrEPs of normal subjects had a consistent shape across conditions and sessions (mean cross correlation waveforms > 0.75). Stroke subjects showed heterogeneous StrEP waveforms. Stroke subjects presented a normal early peak (40 ms after movement onset) but later peaks had abnormal amplitudes and latencies. No significant differences between stroke subjects with good and poor motor function were found (P > 0.14). With the consistent responses of normal subjects the StrEP meets a prerequisite for potential clinical value. Recording of StrEPs is feasible even in subacute stroke survivors with poor motor function. How StrEP features relate to clinical phenotypes and recovery needs further investigatio