Proprioceptive input from the jaw muscles and its influence on lapping, chewing, and posture

Experiments are described which define criteria for identifying fusimotor axons discharging in filaments of the masseter nerve in lightly anaesthetized cats. During reflex movements of the jaw two patterns of discharge were observed in different fusimotor fibres. One type, called "sustained," fired at a fairly constant increased rate. The other, called "modulated," fired at high frequencies during the extrafusal muscle contraction. Evidence from spindle primary and secondary recordings in similar experiments strongly suggests that the "sustained" type were dynamic fusimotor fibres and the "modulated" type were static fusimotor fibres. New spindle recordings in normal unanaesthetized cats indicate that the modulated pattern of static fusimotor discharge also occurs in these conditions. Its effect is to reduce the tendency for spindle afferents to become silent during muscle shortening. A proposal is made that the static fusimotor discharge in cyclic movements may represent a temporal "template" for the intended movement as directed by the central pattern generator.     

The Tuning of Human Motor Response to Risk in a Dynamic Environment Task

The role of motor uncertainty in discrete or static space tasks, such as pointing tasks, has been investigated in many experiments. These studies have shown that humans hold an internal representation of intrinsic and extrinsic motor uncertainty and compensate for this variability when planning movement. The aim of this study was to investigate how humans respond to uncertainties during movement execution in a dynamic environment despite indeterminate knowledge of the outcome of actions. Additionally, the role of errors, or lack thereof, in predicting risk was examined. In the experiment, subjects completed a driving simulation game on a two-lane road. The road contained random curves so that subjects were forced to use sensory feedback to complete the task and could not rely only on motor planning. Risk was manipulated by using horizontal perturbations to create the illusion of driving on a bumpy road, thereby imposing motor uncertainty, and altering the cost function of the road. Results suggest continual responsiveness to cost and uncertainty in a dynamic task and provide evidence that subjects avoid risk even in the absence of errors. The results suggest that humans tune their statistical motor behavior based on cost, taking into account probabilities of possible outcomes in response to environmental uncertainty.     

Effect of motor stimulation and stretching on afferent activity of the neuromuscular spindle isolated from the frog]

The arrangement of muscle spindles in m. ext. long. dig. IV has been examined by microdissection. It is confirmed that spindle systems generally appear to consist of individual receptors. Stimulation effects of fast motor fibres (conduction velocities greater than 12 m/sec) on the spindles of the same muscle were studied. Receptors were isolated with their nerves and the appropriate spinal roots, the latter ones were used for stimulating efferent fibres and recording sensory discharges. Single shocks to the ventral root filaments caused afferent responses ranging from a single action potential to a train of impulses. During repetitive stimulation (train of stimuli at frequency of 10 to 150/sec) a marked increase in afferent activity was found. Afferent activity could be driven by the frequency of stimuli ("driving") and the stimulus/action potentials ratio varied from 1:1 to 1:3 or more. The rate of sensory discharge depended on the frequency of stimuli: the maximum effect, was attained at 30 to 50 stimuli/sec and, in the most responsive receptors, up to 80 stimuli/sec. Slight increases of the initial lengths of the receptors caused facilitation of sensory responses to motor stimulation. Moreover, impairing effects, which appear during sustained or high-frequency stimulation, possibly related to fatigue in intrafusal neuromuscular transmission, could be relieved by increasing the initial length. The repetitive stimulation of fast fusimotor fibres increased both dynamic and static responses and also raised the afferent activity after a period of stretching, when usually a depression occurs; these effects varied according to the preparation, its initial tension and the frequency of stimulation. The main feature of the examined motor fibres, when stimulated, is the constant excitatory action on muscle spindle static response. Results are discussed. It is suggested that the different characteristics of intrafusal muscle fibres, the receptor initial tension and the frequency of motor units discharges, may together affect muscle spindles static or dynamic performance.     

The hyperpolarization-activated HCN1 channel is important for motor learning and neuronal integration by cerebellar Purkinje cells

In contrast to our increasingly detailed understanding of how synaptic plasticity provides a cellular substrate for learning and memory, it is less clear how a neuron's voltage-gated ion channels interact with plastic changes in synaptic strength to influence behavior. We find, using generalized and regional knockout mice, that deletion of the HCN1 channel causes profound motor learning and memory deficits in swimming and rotarod tasks. In cerebellar Purkinje cells, which are a key component of the cerebellar circuit for learning of correctly timed movements, HCN1 mediates an inward current that stabilizes the integrative properties of Purkinje cells and ensures that their input-output function is independent of the previous history of their activity. We suggest that this nonsynaptic integrative function of HCN1 is required for accurate decoding of input patterns and thereby enables synaptic plasticity to appropriately influence the performance of motor activity.     

Optimal response of eye and hand motor systems in pointing at a visual target

The closed loop situation of hand pointing at a target has been experimentally divided into its static and dynamic components. When the subjects see their hand at first (closed loop) until the start of the hand movement cuts off the vision of the hand (open loop), the pointing is significantly more accurate than when it is performed without any vision of the hand before and throughout the movement (fully open loop). This suggests that initial cues as regards hand and target position, improve the motor program by a better identification of initial and final states. As poor as it is, the extra retinal signal (encoding of eye position) improves performance when the foveation is done under closed loop; it allows a better redefinition of target position, and thus modulates the hand motor program through a direct central pathway, which is quicker than the processing of the visual feedback of the hand movement error.     

The representation of time for motor learning

We have identified factors that control precise motor timing by studying learning in smooth pursuit eye movements. Monkeys tracked a target that moved horizontally for a fixed time interval before changing direction through the addition of a vertical component of motion. After repeated presentations of the same target trajectory, infrequent probe trials of purely horizontal target motion evoked a vertical eye movement around the time when the change in target direction would have occurred. The pursuit system timed the vertical eye movement by keeping track of the duration of horizontal target motion and by measuring the distance the target traveled before changing direction, but not by learning the position in space where the target changed direction. We conclude that high temporal precision in motor output relies on multiple signals whose contributions to timing vary according to task requirements.     

Neuronal correlates of the motor function of the cerebral motor cortex

Modern ideas about the motor cortex neuronal mechanisms ensuring the initiation and correction of the instrumental manipulational movements in mammals have been analysed. A close correlation has been established to exist between the neuronal activity and various characteristics of movement including those that are not induced by muscle force. The role of somatic afferentation in the formation and realization of the movement programme is analysed as well as in motor output modulation by means of fast feedback.     

Lateral hop movement assesses ankle dynamics and muscle activity

Ankle function is frequently measured using static or dynamic tasks in normal and injured patients. The purpose of this study was to develop a novel task to quantify ankle dynamics and muscle activity in normal subjects. Twelve subjects with no prior ankle injuries participated. Video motion analysis cameras, force platforms, and an EMG system were used to collect data during a lateral hop movement task that consisted of multiple lateral-medial hops over an obstacle. Mean (SD) inversion ankle position at contact was 4.4° (4.0) in the medial direction and -3.5° (4.4) in the lateral direction; mean (SD) tibialis anterior normalized muscle activity was 0.11 (0.08) in the medial direction and 0.16 (0.13) in the lateral direction. The lateral hop movement was shown to be an effective task for quantifying ankle kinematics, forces, moments, and muscle activities in normal subjects. Future applications will use the lateral hop movement to assess subjects with previous ankle injuries in laboratory and clinical settings.     

Emergence of gamma motor activity in an artificial neural network model of the corticospinal system

Muscle spindle discharge during active movement is a function of mechanical and neural parameters. Muscle length changes (and their derivatives) represent its primary mechanical, fusimotor drive its neural component. However, neither the action nor the function of fusimotor and in particular of γ-drive, have been clearly established, since γ-motor activity during voluntary, non-locomotor movements remains largely unknown. Here, using a computational approach, we explored whether γ-drive emerges in an artificial neural network model of the corticospinal system linked to a biomechanical antagonist wrist simulator. The wrist simulator included length-sensitive and γ-drive-dependent type Ia and type II muscle spindle activity. Network activity and connectivity were derived by a gradient descent algorithm to generate reciprocal, known target α-motor unit activity during wrist flexion-extension (F/E) movements. Two tasks were simulated: an alternating F/E task and a slow F/E tracking task. Emergence of γ-motor activity in the alternating F/E network was a function of α-motor unit drive: if muscle afferent (together with supraspinal) input was required for driving α-motor units, then γ-drive emerged in the form of α-γ coactivation, as predicted by empirical studies. In the slow F/E tracking network, γ-drive emerged in the form of α-γ dissociation and provided critical, bidirectional muscle afferent activity to the cortical network, containing known bidirectional target units. The model thus demonstrates the complementary aspects of spindle output and hence γ-drive: i) muscle spindle activity as a driving force of α-motor unit activity, and ii) afferent activity providing continuous sensory information, both of which crucially depend on γ-drive.     

Different motor learning effects on excitability changes of motor cortex in muscle contraction state

Abstract

We aimed to investigate whether motor learning induces different excitability changes in the human motor cortex (M1) between two different muscle contraction states (before voluntary contraction [static] or during voluntary contraction [dynamic]). For the same, using motor evoked potentials (MEPs) obtained by transcranial magnetic stimulation (TMS), we compared excitability changes during these two states after pinch-grip motor skill learning. The participants performed a force output tracking task by pinch grip on a computer screen. TMS was applied prior to the pinch grip (static) and after initiation of voluntary contraction (dynamic). MEPs of the following muscles were recorded: first dorsal interosseous (FDI), thenar muscle (Thenar), flexor carpi radialis (FCR), and extensor carpi radialis (ECR) muscles. During both the states, motor skill training led to significant improvement of motor performance. During the static state, MEPs of the FDI muscle were significantly facilitated after motor learning; however, during the dynamic state, MEPs of the FDI, Thenar, and FCR muscles were significantly decreased. Based on the results of this study, we concluded that excitability changes in the human M1 are differentially influenced during different voluntary contraction states (static and dynamic) after motor learning.     

Corticospinal Excitability of Trunk Muscles during Different Postural Tasks

Evidence suggests that the primary motor cortex (M1) is involved in both voluntary, goal-directed movements and in postural control. Trunk muscles are involved in both tasks, however, the extent to which M1 controls these muscles in trunk flexion/extension (voluntary movement) and in rapid shoulder flexion (postural control) remains unclear. The purpose of this study was to investigate this question by examining excitability of corticospinal inputs to trunk muscles during voluntary and postural tasks. Twenty healthy adults participated. Transcranial magnetic stimulation was delivered to the M1 to examine motor evoked potentials (MEPs) in the trunk muscles (erector spinae (ES) and rectus abdominis (RA)) during dynamic shoulder flexion (DSF), static shoulder flexion (SSF), and static trunk extension (STE). The level of background muscle activity in the ES muscles was matched across tasks. MEP amplitudes in ES were significantly larger in DSF than in SSF or in STE; however, this was not observed for RA. Further, there were no differences in levels of muscle activity in RA between tasks. Our findings reveal that corticospinal excitability of the ES muscles appears greater during dynamic anticipatory posture-related adjustments than during static tasks requiring postural (SSF) and goal-directed voluntary (STE) activity. These results suggest that task-oriented rehabilitation of trunk muscles should be considered for optimal transfer of therapeutic effect to function.     

The discontinuous nature of motor execution II. Merging discrete and rhythmic movements in a single-joint system -- the phase entrainment effect

 Initiation of rapid discrete flexion movements is significantly altered when a secondary rhythmic movement is performed simultaneously with the same limb; the onset of a stimulus-evoked discrete movement tends to occur time-locked to the oscillation: i.e., the rhythmic movement entrains the discrete response. This nonlinear interaction may reflect a specific principle of coordination of motor tasks which are simultaneously executed with the same effector. This part II of a tripartite research report on such single-muscle multiple-task coordination investigates the contribution of the dynamic properties of the muscle and its reflex circuitry to phase entrainment. Assuming a simple threshold-linear relationship between the control signals generated by the central nervous system and the observable kinematic and electromyographic signals, a secondary rhythmic movement will cause an additional phase-dependent delay between the central “go” command and the first observable change in actual kinematics of the compound movement. Several indicators for such threshold-linear interaction are derived and tested on real data obtained in psychophysical experiments. Four healthy subjects performed rapid lateral abductions of the index finger in response to a visual “go” signal. During a portion of the experiments, subjects produced additional low-amplitude oscillatory movements before stimulus presentation with either the same finger (one-handed task), or with the index finger of the other hand (two-handed task). Results showed phase entrainment and modulation of reaction times when the cyclic and the discrete movements were simultaneously executed by the same finger. But there was no entrainment in the bimanual execution of the tasks. The model was capable of reproducing the observed effects. It is concluded that coordination of voluntary movements which are concurrently performed by the same effector involves specific discontinuous operations, which represents an essential part of the mechanism of motor coordination. Phase entrainment reflects this characteristic discontinuous behavior of the lower stages of motor execution and does not necessarily require nonlinear interaction of motor commands at higher levels of motor processing. Received: 5 September 2001 / Accepted in revised form: 19 December 2001     

Different fusimotor reflexes from the ipsi- and contralateral hind limbs of the cat assessed in the same primary muscle spindle afferents

Experiments were performed in forty-five cats anaesthetized with alpha-chloralose. The aim of the study was to investigate a sample of primary muscle spindle afferents from triceps muscle with respect to their fusimotor reflex control from ipsi- as well as contralateral hind limb. Primary muscle spindle afferents of the triceps surae muscle were recorded from the mean rate of firing and the modulation of the afferent response to sinusoidal stretching of the triceps surae muscle was determined. Test measurements were made during tonic stretch of the ipsilateral PBSt, contralateral PBSt, contralateral triceps muscle or during extension of the intact contralateral hind limb. Control measurements were made with ipsi- and contralateral PBSt as well as contralateral triceps muscles relaxed and with contralateral hind limb in resting position. The occurrence and types of fusimotor effects were assessed by comparing test to control responses. The main finding of the present investigation was the great variability in type and size of the fusimotor effects evoked by different ipsi- and contralateral reflex stimuli. Both ipsi- and contralateral stimulations gave rise to predominantly dynamic, predominantly static or mixed static and dynamic fusimotor reflexes. In the same preparation, a given reflex stimulus often caused different reflex responses in different triceps surae primary spindle afferents. In the same afferent unit, different reflex stimuli usually produced fusimotor effects which differed from each other in type and/or size. In general, contralateral whole limb extension and stretch of contralateral PBSt muscles were more potent as reflex stimuli than stretch of the ipsilateral PBSt muscle. Stretch of the contralateral triceps surae muscle was, but for a few afferent units, ineffective as reflexogenic stimulus. It is concluded that the individualized receptive profiles of the primary muscle spindle afferents, which have been postulated in earlier investigations where the effects of different stimuli have been investigated on different cell populations, still seems to hold good when the stimuli are tested on the same units. The individuality of the receptive profiles of gamma-motoneurones is discussed in relation to different motor control hypotheses.     

Model-based prediction of fusimotor activity and its effect on muscle spindle activity during voluntary wrist movements

Muscle spindles provide critical information about movement position and velocity. They have been shown to act as stretch receptors in passive muscle, however, during active movements their behavior is less clear. In particular, spindle responses have been shown to be out-of-phase or phase advanced with respect to their expected muscle length-sensitivity. Whether this apparent discrepancy of spindle responses between passive and active movements is due to fusimotor (γ-drive) remains unresolved, since the activity of fusimotor neurons during voluntary non-locomotor movements are largely unknown. We developed a computational model to predict fusimotor activity and to investigate whether fusimotor activity could explain the empirically observed phase advance of spindle responses. The model links a biomechanical wrist model to length- and γ-drive-dependent transfer functions of type Ia and type II muscle spindle activity. Our simulations of two wrist-movement tasks suggest that (i) experimentally observed type Ia and type II activity profiles can to a large part be explained by appropriate, i.e. strongly modulated and task-dependent, γ-drive. That (ii) the empirically observed phase advance of type Ia or of type II profiles during active movement can be similarly explained by appropriate γ-drive. In summary, the simulation predicts that a highly task-modulated activation of the γ-system is instrumental in producing a large part of the empirically observed muscle spindle activity for voluntary wrist movements.     

Modeling of a simple motor task in man: intentional arrest of an ongoing movement

Normal subjects and cerebellar patients were instructed to arrest “as soon as possible” a ballistically initiated flexion movement of the forearm. The intentional actions consist essentially of a downward torque, the peak value of which has almost a constant latency (about 200 msec) from the beginning of the movement. A variable number of oscillations precede the arrest of the movement, the characteristics of which depend on the initial velocity of the flexion and on the mass with which the forearm is loaded. The motor commands responsible for the intentionally produced downward torque are controlled centrally as to leave the ratio between the peak values of the angular velocity which precede and follow the peak of the torque almost constant, under all conditions. To describe the oscillations a simple analytical model was proposed which includes the mechanical as well as the reflex factors, the latter under the form of a delayed velocity term. The satisfactory fitting of this model to the experimental findings permitted to establish the following points:

1. The oscillations are sustained by both a mechanical and a reflex stiffness. The contribution of the reflex loop is however quantitatively dominant since it accounts for about 75% of the inertial torque. It is fairly constant over the range of frequency of the oscillations considered.
2. Under the imposed experimental conditions angular velocity appears to be the parameter of the movement which is predominantly sensed and fed back by the reflex loop.

Data were also presented on the performance of the motor task by patients who underwent surgical ablations of the cerebellar cortex. Comparison of these results with those of normal subjects strongly supports the hypothesis that cerebellar-related activities are instrumental in determining the sensitivity of the stretch reflex to angular velocity.     

Correlations between activity of pallidal neurons and motor parameters

Abstract The relationships between the activity of 87 pallidal neurons and parameters characterizing motor performance were analysed quantitatively in six unrestrained cats performing a forelimb flexion movement controlled by a reaction-time paradigm. Three motor variables were considered: the static force exerted when the trigger stimulus occurred, the latency of the force change initiating the lever-release movement and the velocity of the force change. For all the cats, the latency of the change in force was the prevalent parameter in determining the movement onset occurrence. The single-unit activity was quantified on a trial-by-trial basis by measuring the mean firing rate in windows of fixed duration. Both normal (total) and partial linear correlation coefficients were used. Partial correlation coefficients were calculated between the mean firing rate during selected windows and each of the motor parameters. A total of 17% and 9% of all partial correlation coefficients tested ( n = 1566) was found to be significantly different from zero, respectively with p 0.05 and p 0.01. The mean percentages of explained variation, measured by the square of the correlation coefficient, were 17% ( p 0.05) and 21% ( p 0.01). The 46 pallidal neurons presenting an increase in discharge after the trigger stimulus could be classified in homogeneous subgroups with respect to the signs of the correlations. Representations of the motor programme underlying reaction-time performance evidenced at the pallidal level further substantiate a specific involvement of the basal ganglia in the latency of motor triggering.     

Cerebral activations related to ballistic, stepwise interrupted and gradually modulated movements in Parkinson patients

Patients with Parkinson’s disease (PD) experience impaired initiation and inhibition of movements such as difficulty to start/stop walking. At single-joint level this is accompanied by reduced inhibition of antagonist muscle activity. While normal basal ganglia (BG) contributions to motor control include selecting appropriate muscles by inhibiting others, it is unclear how PD-related changes in BG function cause impaired movement initiation and inhibition at single-joint level. To further elucidate these changes we studied 4 right-hand movement tasks with fMRI, by dissociating activations related to abrupt movement initiation, inhibition and gradual movement modulation. Initiation and inhibition were inferred from ballistic and stepwise interrupted movement, respectively, while smooth wrist circumduction enabled the assessment of gradually modulated movement. Task-related activations were compared between PD patients (N = 12) and healthy subjects (N = 18). In healthy subjects, movement initiation was characterized by antero-ventral striatum, substantia nigra (SN) and premotor activations while inhibition was dominated by subthalamic nucleus (STN) and pallidal activations, in line with the known role of these areas in simple movement. Gradual movement mainly involved antero-dorsal putamen and pallidum. Compared to healthy subjects, patients showed reduced striatal/SN and increased pallidal activation for initiation, whereas for inhibition STN activation was reduced and striatal-thalamo-cortical activation increased. For gradual movement patients showed reduced pallidal and increased thalamo-cortical activation. We conclude that PD-related changes during movement initiation fit the (rather static) model of alterations in direct and indirect BG pathways. Reduced STN activation and regional cortical increased activation in PD during inhibition and gradual movement modulation are better explained by a dynamic model that also takes into account enhanced responsiveness to external stimuli in this disease and the effects of hyper-fluctuating cortical inputs to the striatum and STN in particular.     

Activity of fusimotor neurons during reflex muscle contraction

The influence of fusimotor activity via the gamma-loop on reflex responses of motoneurons to stretch or vibration stimulation of mm. triceps surae was studied in decerebrate cats. Action potentials of single fusimotor neurons were derived from thin filaments isolated from nerves innervating this muscle group, leaving their main nerve supply intact. Most fusimotor neurons tested were found to be coactivated with motor units during reflex muscle contraction. In the initial period of development of reflex muscle contraction a weak autogenetic inhibitory effect on discharge of fusimotor neurons was found. The results suggest that reduction of the reflex motor signal, leading to a "silent period," is partly the result of a transient decrease in the fusimotor output effect on contracting muscles. A study of changes in fusimotor discharge generation during the ascending phase of reflex muscle contraction may provide data useful for identification of autogenetic reflex influences on these motoneurons and for elucidating the conditions necessary for servoassistance of muscle contractions.Medical Research Institute, Belgrade, Yugoslavia. Translated from Neirofiziologiya, Vol. 16, No. 5, pp. 630–637, September–October, 1984.     

Combining frequency and time domain approaches to systems with multiple spike train input and output

A frequency domain approach and a time domain approach have been combined in an investigation of the behaviour of the primary and secondary endings of an isolated muscle spindle in response to the activity of two static fusimotor axons when the parent muscle is held at a fixed length and when it is subjected to random length changes. The frequency domain analysis has an associated error process which provides a measure of how well the input processes can be used to predict the output processes and is also used to specify how the interactions between the recorded processes contribute to this error. Without assuming stationarity of the input, the time domain approach uses a sequence of probability models of increasing complexity in which the number of input processes to the model is progressively increased. This feature of the time domain approach was used to identify a preferred direction of interaction between the processes underlying the generation of the activity of the primary and secondary endings. In the presence of fusimotor activity and dynamic length changes imposed on the muscle, it was shown that the activity of the primary and secondary endings carried different information about the effects of the inputs imposed on the muscle spindle. The results presented in this work emphasise that the analysis of the behaviour of complex systems benefits from a combination of frequency and time domain methods. This article is part of a special issue on Neuronal Dynamics of Sensory Coding.     

The discontinuous nature of motor execution

Human movement control requires adequate coordination of different movements, which is particularly important when different motor tasks are simultaneously executed by the same effector(s) (e.g. a muscle or a joint). The process of movement execution involves a series of highly nonlinear elements; for instance, a motor unit of a muscle produces force only in the direction of muscle shortening, thus representing a threshold operator that transforms the bipolar (i.e. excitatory or inhibitory) information at its spinal input into a purely unipolar signal (i.e. muscle force). This tripartite research report addresses the contribution of the nonlinearity of neuromuscular elements to the coordination of different motor tasks simultaneously executed by the same limb. In this first part of the series, a new hypothesis for such a single-muscle multiple-task coordination is presented which suggests an essentially threshold-linear coordination mechanism. Control signals generated by the central nervous system for each individual movement independently and feedback information from peripheral receptors are linearly superimposed. This compound control/feedback signal is processed by a nonlinear limiter element reflecting the discontinuous properties of the muscle and its reflex circuitry. It is shown that threshold-linear interaction of descending commands and afferent feedback information can lead to complex interdependent patterns of compound motor action. This includes the possibility of gating (i.e. the ability of one movement pattern to constrain or even impede the execution of another pattern) and of delayed response initiation when simultaneously performing more than one voluntary motor task. A theoretical analysis of the threshold-linear coordination mechanism and an extensive experimental validation of the model is provided in part II and part III of the report. Received: 6 October 1998 / Accepted in revised form: 2 June 1999