Early stages of sensorimotor map acquisition: neurochemical signature in primary motor cortex and its relation to functional connectivity.

The earliest stages of sensorimotor learning involve learning the correspondence between movements and sensory results-a sensorimotor map. The present exploratory study investigated the neurochemical underpinnings of map acquisition by monitoring 25 participants as they acquired a new association between movements and sounds. Functional magnetic resonance spectroscopy was used to measure neurochemical concentrations in the left primary motor cortex during learning. Resting-state functional magnetic resonance imaging data were also collected before and after training to assess learning-related changes in functional connectivity. There were monotonic increases in γ-aminobutyric acid (GABA) and decreases in glucose during training, which extended into the subsequent rest period and, importantly, in the case of GABA correlated with the amount of learning: participants who showed greater behavioral learning showed greater GABA increase. The GABA change was furthermore correlated with changes in functional connectivity between the primary motor cortex and a cluster of voxels in the right intraparietal sulcus: greater increases in GABA were associated with greater strengthening of connectivity. Transiently, there were increases in lactate and reductions in aspartate, which returned to baseline at the end of training, but only lactate showed a statistical trend to correlate with the amount of learning. In summary, during the earliest stages of sensorimotor learning, GABA levels are linked on a subject-level basis to both behavioral learning and a strengthening of functional connections that persists beyond the training period. The findings are consistent with the idea that GABA-mediated inhibition is linked to maintenance of newly learned information.NEW & NOTEWORTHY Learning the mapping between movements and their sensory effects is a necessary step in the early stages of sensorimotor learning. There is evidence showing which brain areas are involved in early motor learning, but their role remains uncertain. Here, we show that GABA, a neurotransmitter linked to inhibitory processing, rises during and after learning and is involved in ongoing changes in resting-state networks.

Early stages of sensorimotor map acquisition: learning with free exploration, without active movement or global structure.

One of the puzzles of learning to talk or play a musical instrument is how we learn which movement produces a particular sound: an audiomotor map. The initial stages of map acquisition can be studied by having participants learn arm movements to auditory targets. The key question is what mechanism drives this early learning. Three learning processes from previous literature were tested: map learning may rely on active motor outflow (target), on error correction, and on the correspondence between sensory and motor distances (i.e., that similar movements map to similar sounds). Alternatively, we hypothesized that map learning can proceed without these. Participants made movements that were mapped to sounds in a number of different conditions that each precluded one of the potential learning processes. We tested whether map learning relies on assumptions about topological continuity by exposing participants to a permuted map that did not preserve distances in auditory and motor space. Further groups were tested who passively experienced the targets, kinematic trajectories produced by a robot arm, and auditory feedback as a yoked active participant (hence without active motor outflow). Another group made movements without receiving targets (thus without experiencing errors). In each case we observed substantial learning, therefore none of the three hypothesized processes is required for learning. Instead early map acquisition can occur with free exploration without target error correction, is based on sensory-to-sensory correspondences, and possible even for discontinuous maps. The findings are consistent with the idea that early sensorimotor map formation can involve instance-specific learning.NEW & NOTEWORTHY This study tested learning of novel sensorimotor maps in a variety of unusual circumstances, including learning a mapping that was permuted in such as way that it fragmented the sensorimotor workspace into discontinuous parts, thus not preserving sensory and motor topology. Participants could learn this mapping, and they could learn without motor outflow or targets. These results point to a robust learning mechanism building on individual instances, inspired from machine learning literature.

Relationship between cocontraction, movement kinematics and phasic muscle activity in single-joint arm movement.

Patterns of muscle coactivation provide a window into mechanisms of limb stabilization. In the present paper we have examined muscle coactivation in single-joint elbow and single-joint shoulder movements and explored its relationship to movement velocity and amplitude, as well as phasic muscle activation patterns. Movements were produced at several speeds and different amplitudes, and muscle activity and movement kinematics were recorded. Tonic levels of electromyographic (EMG) activity following movement provided a measure of muscle cocontraction. It was found that coactivation following movement increased with maximum joint velocity at each of two amplitudes. Phasic EMG activity in agonist and antagonist muscles showed a similar correlation that was observable even during the first 30 ms of muscle activation. All subjects but one showed statistically significant correlations on a trial-by-trial basis between tonic and phasic activity levels, including the phasic activity measure taken at the initiation of movement. Our findings provide direct evidence that muscle coactivation varies with movement velocity. The data also suggest that cocontraction is linked in a simple manner to phasic muscle activity. The similarity in the patterns of tonic and phasic activation suggests that the nervous system may use a simple strategy to adjust coactivation and presumably limb impedance in association with changes in movement speed. Moreover, since the pattern of tonic activity varies with the first 30 ms of phasic activity, the control of cocontraction may be established prior to movement onset.

Tactile shape processing.

Neuroimaging techniques may aid in the identification of areas of the human brain that are involved in tactile shape perception. Bodegård et al. (2001) relate differences in the properties of tactile stimuli to differences in areas of cortical activation to infer tactile processing in the somatosensory network.

Compensation for the effects of head acceleration on jaw movement in speech.

Recent studies have demonstrated the ability of subjects to adjust the control of limb movements to counteract the effects of self-generated loads. The degree to which subjects change control signals to compensate for these loads is a reflection of the extent to which forces affecting movement are represented in motion planning. Here, we have used empirical and modeling studies to examine whether the nervous system compensates for loads acting on the jaw during speech production. As subjects walk, loads to the jaw vary with the direction and magnitude of head acceleration. We investigated the patterns of jaw motion resulting from these loads both in locomotion alone and when locomotion was combined with speech production. In locomotion alone, jaw movements were shown to vary systematically in direction and magnitude in relation to the acceleration of the head. In contrast, when locomotion was combined with speech, variation in jaw position during both consonant and vowel production was substantially reduced. Overall, we have demonstrated that the magnitude of load associated with head acceleration during locomotion is sufficient to produce a systematic change in the position of the jaw. The absence of variation in jaw position during locomotion with speech is thus consistent with the idea that in speech, the control of jaw motion is adjusted in a predictive manner to offset the effects of head acceleration.

Compensation for loads during arm movements using equilibrium-point control.

A significant problem in motor control is how information about movement error is used to modify control signals to achieve desired performance. A potential source of movement error and one that is readily controllable experimentally relates to limb dynamics and associated movement-dependent loads. In this paper, we have used a position control model to examine changes to control signals for arm movements in the context of movement-dependent loads. In the model, based on the equilibrium-point hypothesis, equilibrium shifts are adjusted directly in proportion to the positional error between desired and actual movements. The model is used to simulate multi-joint movements in the presence of both "internal" loads due to joint interaction torques, and externally applied loads resulting from velocity-dependent force fields. In both cases it is shown that the model can achieve close correspondence to empirical data using a simple linear adaptation procedure. An important feature of the model is that it achieves compensation for loads during movement without the need for either coordinate transformations between positional error and associated corrective forces, or inverse dynamics calculations.

Compensation for interaction torques during single- and multijoint limb movement.

During multijoint limb movements such as reaching, rotational forces arise at one joint due to the motions of limb segments about other joints. We report the results of three experiments in which we assessed the extent to which control signals to muscles are adjusted to counteract these "interaction torques." Human subjects performed single- and multijoint pointing movements involving shoulder and elbow motion, and movement parameters related to the magnitude and direction of interaction torques were manipulated systematically. We examined electromyographic (EMG) activity of shoulder and elbow muscles and, specifically, the relationship between EMG activity and joint interaction torque. A first set of experiments examined single-joint movements. During both single-joint elbow (experiment 1) and shoulder (experiment 2) movements, phasic EMG activity was observed in muscles spanning the stationary joint (shoulder muscles in experiment 1 and elbow muscles in experiment 2). This muscle activity preceded movement and varied in amplitude with the magnitude of upcoming interaction torque (the load resulting from motion of the nonstationary limb segment). In a third experiment, subjects performed multijoint movements involving simultaneous motion at the shoulder and elbow. Movement amplitude and velocity at one joint were held constant, while the direction of movement about the other joint was varied. When the direction of elbow motion was varied (flexion vs. extension) and shoulder kinematics were held constant, EMG activity in shoulder muscles varied depending on the direction of elbow motion (and hence the sign of the interaction torque arising at the shoulder). Similarly, EMG activity in elbow muscles varied depending on the direction of shoulder motion for movements in which elbow kinematics were held constant. The results from all three experiments support the idea that central control signals to muscles are adjusted, in a predictive manner, to compensate for interaction torques-loads arising at one joint that depend on motion about other joints.

Effects of gravitational load on jaw movements in speech.

External loads arising as a result of the orientation of body segments relative to gravity can affect the achievement of movement goals. The degree to which subjects adjust control signals to compensate for these loads is a reflection of the extent to which forces affecting motion are represented neurally. In the present study we assessed whether subjects, when speaking, compensate for loads caused by the orientation of the head relative to gravity. We used a mathematical model of the jaw to predict the effects of control signals that are not adjusted for changes to head orientation. The simulations predicted a systematic change in sagittal plane jaw orientation and horizontal position resulting from changes to the orientation of the head. We conducted an empirical study in which subjects were tested under the same conditions. With one exception, empirical results were consistent with the simulations. In both simulation and empirical studies, the jaw was rotated closer to occlusion and translated in an anterior direction when the head was in the prone orientation. When the head was in the supine orientation, the jaw was rotated away from occlusion. The findings suggest that the nervous system does not completely compensate for changes in head orientation relative to gravity. A second study was conducted to assess possible changes in acoustical patterns attributable to changes in head orientation. The frequencies of the first (F1) and second (F2) formants associated with the steady-state portion of vowels were measured. As in the kinematic study, systematic differences in the values of F1 and F2 were observed with changes in head orientation. Thus the acoustical analysis further supports the conclusion that control signals are not completely adjusted to offset forces arising because of changes in orientation.

Independent coactivation of shoulder and elbow muscles.

The aim of this study was to examine the possibility of independent muscle coactivation at the shoulder and elbow. Subjects performed rapid point-to-point movements in a horizontal plane from different initial limb configurations to a single target. EMG activity was measured from flexor and extensor muscles acting at the shoulder (pectoralis clavicular head and posterior deltoid) and elbow (biceps long head and triceps lateral head) and flexor and extensor muscles acting at both joints (biceps short head and triceps long head). Muscle coactivation was assessed by measuring tonic levels of electromyographic (EMG) activity after limb position stabilized following the end of the movements. It was observed that tonic EMG levels following movements to the same target varied as a function of the amplitude of shoulder and elbow motion. Moreover, for the movements tested here, the coactivation of shoulder and elbow muscles was found to be independent - tonic EMG activity of shoulder muscles increased in proportion to shoulder movement, but was unrelated to elbow motion, whereas elbow and double-joint muscle coactivation varied with the amplitude of elbow movement and were not correlated with shoulder motion. In addition, tonic EMG levels were higher for movements in which the shoulder and elbow rotated in the same direction than for those in which the joints rotated in opposite directions. In this respect, muscle coactivation may reflect a simple strategy to compensate for forces introduced by multijoint limb dynamics.

Recent tests of the equilibrium-point hypothesis (lambda model).

The lambda model of the equilibrium-point hypothesis (Feldman & Levin, 1995) is an approach to motor control which, like physics, is based on a logical system coordinating empirical data. The model has gone through an interesting period. On one hand, several nontrivial predictions of the model have been successfully verified in recent studies. In addition, the explanatory and predictive capacity of the model has been enhanced by its extension to multimuscle and multijoint systems. On the other hand, claims have recently appeared suggesting that the model should be abandoned. The present paper focuses on these claims and concludes that they are unfounded. Much of the experimental data that have been used to reject the model are actually consistent with it.

Are complex control signals required for human arm movement?

It has been proposed that the control signals underlying voluntary human arm movement have a "complex" nonmonotonic time-varying form, and a number of empirical findings have been offered in support of this idea. In this paper, we address three such findings using a model of two-joint arm motion based on the lambda version of the equilibrium-point hypothesis. The model includes six one- and two-joint muscles, reflexes, modeled control signals, muscle properties, and limb dynamics. First, we address the claim that "complex" equilibrium trajectories are required to account for nonmonotonic joint impedance patterns observed during multijoint movement. Using constant-rate shifts in the neurally specified equilibrium of the limb and constant cocontraction commands, we obtain patterns of predicted joint stiffness during simulated multijoint movements that match the nonmonotonic patterns reported empirically. We then use the algorithm proposed by Gomi and Kawato to compute a hypothetical equilibrium trajectory from simulated stiffness, viscosity, and limb kinematics. Like that reported by Gomi and Kawato, the resulting trajectory was nonmonotonic, first leading then lagging the position of the limb. Second, we address the claim that high levels of stiffness are required to generate rapid single-joint movements when simple equilibrium shifts are used. We compare empirical measurements of stiffness during rapid single-joint movements with the predicted stiffness of movements generated using constant-rate equilibrium shifts and constant cocontraction commands. Single-joint movements are simulated at a number of speeds, and the procedure used by Bennett to estimate stiffness is followed. We show that when the magnitude of the cocontraction command is scaled in proportion to movement speed, simulated joint stiffness varies with movement speed in a manner comparable with that reported by Bennett. Third, we address the related claim that nonmonotonic equilibrium shifts are required to generate rapid single-joint movements. Using constant-rate equilibrium shifts and constant cocontraction commands, rapid single-joint movements are simulated in the presence of external torques. We use the procedure reported by Latash and Gottlieb to compute hypothetical equilibrium trajectories from simulated torque and angle measurements during movement. As in Latash and Gottlieb, a nonmonotonic function is obtained even though the control signals used in the simulations are constant-rate changes in the equilibrium position of the limb. Differences between the "simple" equilibrium trajectory proposed in the present paper and those that are derived from the procedures used by Gomi and Kawato and Latash and Gottlieb arise from their use of simplified models of force generation.

A dynamic biomechanical model for neural control of speech production.

A model of the midsagittal plane motion of the tongue, jaw, hyoid bone, and larynx is presented, based on the lambda version of equilibrium point hypothesis. The model includes muscle properties and realistic geometrical arrangement of muscles, modeled neural inputs and reflexes, and dynamics of soft tissue and bony structures. The focus is on the organization of control signals underlying vocal tract motions and on the dynamic behavior of articulators. A number of muscle synergies or "basic motions" of the system are identified. In particular, it is shown that systematic sources of variation in an x-ray data base of midsagittal vocal tract motions can be accounted for, at the muscle level, with six independent commands, each corresponding to a direction of articulator motion. There are two commands for the jaw (corresponding to sagittal plane jaw rotation and jaw protrusion), one command controlling larynx height, and three commands for the tongue (corresponding to forward and backward motion of the tongue body, arching and flattening of the tongue dorsum, and motion of the tongue tip). It is suggested that all movements of the system can be approximated as linear combinations of such basic motions. In other words, individual movements and sequences of movements can be accounted for by a simple additive control model. The dynamics of individual commands are also assessed. It is shown that the dynamic effects are not neglectable in speechlike movements because of the different dynamic behaviors of soft and bony structures.

A system for three-dimensional visualization of human jaw motion in speech.

With the development of precise three-dimensional motion measurement systems and powerful computers for three-dimensional graphical visualization, it is possible to record and fully reconstruct human jaw motion. In this paper, we describe a visualization system for displaying three-dimensional jaw movements in speech. The system is designed to take as input jaw motion data obtained from one or multi-dimensional recording systems. In the present application, kinematic records of jaw motion were recorded using an optoelectronic measurement system (Optotrak). The corresponding speech signal was recorded using an analog input channel. The three orientation angles and three positions that describe the motion of the jaw as a rigid skeletal structure were derived from the empirical measurements. These six kinematic variables, which in mechanical terms account fully for jaw motion kinematics, act as inputs that drive a real-time three-dimensional animation of a skeletal jaw and upper skull. The visualization software enables the user to view jaw motion from any orientation and to change the viewpoint during the course of an utterance. Selected portions of an utterance may be replayed and the speed of the visual display may be varied. The user may also display, along with the audio track, individual kinematic degrees of freedom or several degrees of freedom in combination. The system is presently being used as an educational tool and for research into audio-visual speech recognition. Interested researchers may obtain the software and source code free of charge from the authors.

Phasic and tonic stretch reflexes in muscles with few muscle spindles: human jaw-opener muscles.

We investigated phasic and tonic stretch reflexes in human jaw-opener muscles, which have few, if any, muscle spindles. Jaw-unloading reflexes were recorded for both opener and closer muscles. Surface electromyographic (EMG) activity was obtained from left and right digastric and superficial masseter muscles, and jaw orientation and torques were recorded. Unloading of jaw-opener muscles elicited a short-latency decrease in EMG activity (averaging 20 ms) followed by a short-duration silent period in these muscles and sometimes a short burst of activity in their antagonists. Similar behavior in response to unloading was observed for spindle-rich jaw-closer muscles, although the latency of the silent period was statistically shorter than that observed for jaw-opener muscles (averaging 13 ms). Control studies suggest that the jaw-opener reflex was not due to inputs from either cutaneous or periodontal mechanoreceptors. In the unloading response of the jaw openers, the tonic level of EMG activity observed after transition to the new jaw orientation was monotonically related to the residual torque and orientation. This is consistent with the idea that the tonic stretch reflex might mediate the change in muscle activation. In addition, the values of the static net joint torque and jaw orientation after the dynamic phase of unloading were related by a monotonic function resembling the invariant characteristic recorded in human limb joints. The torque-angle characteristics associated with different initial jaw orientations were similar in shape but spatially shifted, consistent with the idea that voluntary changes in jaw orientation might be associated with a change in a single parameter, which might be identified as the threshold of the tonic stretch reflex. It is suggested that functionally significant phasic and tonic stretch reflexes might not be mediated exclusively by muscle spindle afferents. Thus, the hypothesis that central modifications in the threshold of the tonic stretch reflex underlie the control of movement may be applied to the jaw system.

An examination of the degrees of freedom of human jaw motion in speech and mastication.

The kinematics of human jaw movements were assessed in terms of the three orientation angles and three positions that characterize the motion of the jaw as a rigid body. The analysis focused on the identification of the jaw's independent movement dimensions, and was based on an examination of jaw motion paths that were plotted in various combinations of linear and angular coordinate frames. Overall, both behaviors were characterized by independent motion in four degrees of freedom. In general, when jaw movements were plotted to show orientation in the sagittal plane as a function of horizontal position, relatively straight paths were observed. In speech, the slopes and intercepts of these paths varied depending on the phonetic material. The vertical position of the jaw was observed to shift up or down so as to displace the overall form of the sagittal plane motion path of the jaw. Yaw movements were small but independent of pitch, and vertical and horizontal position. In mastication, the slope and intercept of the relationship between pitch and horizontal position were affected by the type of food and its size. However, the range of variation was less than that observed in speech. When vertical jaw position was plotted as a function of horizontal position, the basic form of the path of the jaw was maintained but could be shifted vertically. In general, larger bolus diameters were associated with lower jaw positions throughout the movement. The timing of pitch and yaw motion differed. The most common pattern involved changes in pitch angle during jaw opening followed by a phase predominated by lateral motion (yaw). Thus, in both behaviors there was evidence of independent motion in pitch, yaw, horizontal position, and vertical position. This is consistent with the idea that motions in these degrees of freedom are independently controlled.

Origins of the power law relation between movement velocity and curvature: modeling the effects of muscle mechanics and limb dynamics.

1. When subjects trace patterns such as ellipses, the instantaneous velocity of movements is related to the instantaneous curvature of the trajectories according to a power law-movements tend to slow down when curvature is high and speed up when curvature is low. It has been proposed that this relationship is centrally planned. 2. The arm's muscle properties and dynamics can significantly affect kinematics. Even under isometric conditions, muscle mechanical properties can affect the development of muscle forces and torques. Without a model that accounts for these effects, it is difficult to distinguish between kinematic patterns that are attributable to central control and patterns that arise because of dynamics and muscle properties and are not represented in the underlying control signals. 3. In this paper we address the nature of the control signals that underlie movements that obey the power law. We use a numerical simulation of arm movement control based on the lambda version of the equilibrium point hypothesis. We demonstrate that simulated elliptical and circular movements, and elliptical force trajectories generated under isometric conditions, obey the power law even though there was no relation between curvature and speed in the modeled control signals. 4. We suggest that limb dynamics and muscle mechanics-specifically, the springlike properties of muscles-can contribute significantly to the emergence of the power law relationship in kinematics. Thus, without a model that accounts for these effects, care must be taken when making inferences about the nature of neural control.

Specific involvement of human parietal systems and the amygdala in the perception of biological motion.

To explore the extent to which functional systems within the human posterior parietal cortex and the superior temporal sulcus are involved in the perception of action, we measured cerebral metabolic activity in human subjects by positron emission tomography during the perception of simulations of biological motion with point-light displays. The experimental design involved comparisons of activity during the perception of goal-directed hand action, whole body motion, object motion, and random motion. The results demonstrated that the perception of scripts of goal-directed hand action implicates the cortex in the intraparietal sulcus and the caudal part of the superior temporal sulcus, both in the left hemisphere. By contrast, the rostrocaudal part of the right superior temporal sulcus and adjacent temporal cortex, and limbic structures such as the amygdala, are involved in the perception of signs conveyed by expressive body movements.

Functional data analyses of lip motion.

The vocal tract's motion during speech is a complex patterning of the movement of many different articulators according to many different time functions. Understanding this myriad of gestures is important to a number of different disciplines including automatic speech recognition, speech and language pathologies, speech motor control, and experimental phonetics. Central issues are the accurate description of the shape of the vocal tract and determining how each articulator contributes to this shape. A problem facing all of these research areas is how to cope with the multivariate data from speech production experiments. In this paper techniques are described that provide useful tools for describing multivariate functional data such as the measurement of speech movements. The choice of data analysis procedures has been motivated by the need to partition the articulator movement in various ways: end effects separated from shape effects, partitioning of syllable effects, and the splitting of variation within an articulator site from variation from between sites. The techniques of functional data analysis seem admirably suited to the analyses of phenomena such as these. Familiar multivariate procedures such as analysis of variance and principal components analysis have their functional counterparts, and these reveal in a way more suited to the data the important sources of variation in lip motion. Finally, it is found that the analyses of acceleration were especially helpful in suggesting possible control mechanisms. The focus is on using these speech production data to understand the basic principles of coordination. However, it is believed that the tools will have a more general use.

The equilibrium point hypothesis and its application to speech motor control.

In this paper, we address a number of issues in speech research in the context of the equilibrium point hypothesis of motor control. The hypothesis suggests that movements arise from shifts in the equilibrium position of the limb or the speech articulator. The equilibrium is a consequence of the interaction of central neural commands, reflex mechanisms, muscle properties, and external loads, but it is under the control of central neural commands. These commands act to shift the equilibrium via centrally specified signals acting at the level of the motoneurone (MN) pool. In the context of a model of sagittal plane jaw and hyoid motion based on the lambda version of the equilibrium point hypothesis, we consider the implications of this hypothesis for the notion of articulatory targets. We suggest that simple linear control signals may underlie smooth articulatory trajectories. We explore as well the phenomenon of intraarticulator coarticulation in jaw movement. We suggest that even when no account is taken of upcoming context, that apparent anticipatory changes in movement amplitude and duration may arise due to dynamics. We also present a number of simulations that show in different ways how variability in measured kinematics can arise in spite of constant magnitude speech control signals.