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Biomedical subjects

Roland S Johansson

Publications and source records attributed to Roland S Johansson.

16 recordsLinked to original sources

Control strategies in object manipulation tasks.

The remarkable manipulative skill of the human hand is not the result of rapid sensorimotor processes, nor of fast or powerful effector mechanisms. Rather, the secret lies in the way manual tasks are organized and controlled by the nervous system. At the heart of this organization is prediction. Successful manipulation requires the ability both to predict the motor commands required to grasp, lift, and move objects and to predict the sensory events that arise as a consequence of these commands.

Animals↗

Precision grip function after free toe transfer in children with hypoplastic digits.

Although toe-to-hand transfer has a defined role in the management of congenital hand deformities, it remains unclear how well children integrate the transferred digits into physiological grasping. We analysed fingertip forces in the precision grip of 13 patients when lifting a test object more than three years after free toe transfer for absent or hypoplastic digits. Clinically, most patients showed normal sensibility of transferred digits, but active motion and pinch strength were limited as compared to the normal hand. For the control of fingertip forces, two key features of the normal two-digit opposition grip were seen in all operated hands: adaptation of grip force to object weight and parallel coordination of lift and grip forces. These physiological grasping strategies developed independently of the patients' age at the time of operation, which ranged from one to 13 years. In four patients, we observed increased tangential load forces with the operated hand due to misalignments in the application of fingertips on the grasp surfaces. Such forces lead to increased grip force requirements on both fingers that may overload transferred digits with limited motor function. The need for optimal alignment of the grip axis during toe-transfer surgery is emphasised.

Adaptation, Physiological↗

Eye movements when observing predictable and unpredictable actions.

We previously showed that, when observers watch an actor performing a predictable block-stacking task, the coordination between the observer's gaze and the actor's hand is similar to the coordination between the actor's gaze and hand. Both the observer and the actor direct gaze to forthcoming grasp and block landing sites and shift their gaze to the next grasp or landing site at around the time the hand contacts the block or the block contacts the landing site. Here we compare observers' gaze behavior in a block manipulation task when the observers did and when they did not know, in advance, which of two blocks the actor would pick up first. In both cases, observers managed to fixate the target ahead of the actor's hand and showed proactive gaze behavior. However, these target fixations occurred later, relative to the actor's movement, when observers did not know the target block in advance. In perceptual tests, in which observers watched animations of the actor reaching partway to the target and had to guess which block was the target, we found that the time at which observers were able to correctly do so was very similar to the time at which they would make saccades to the target block. Overall, our results indicate that observers use gaze in a fashion that is appropriate for hand movement planning and control. This in turn suggests that they implement representations of the manual actions required in the task and representations that direct task-specific eye movements.

Adult↗

How a lateralized brain supports symmetrical bimanual tasks.

A large repertoire of natural object manipulation tasks require precisely coupled symmetrical opposing forces by both hands on a single object. We asked how the lateralized brain handles this basic problem of spatial and temporal coordination. We show that the brain consistently appoints one of the hands as prime actor while the other assists, but the choice of acting hand is flexible. When study participants control a cursor by manipulating a tool held freely between the hands, the left hand becomes prime actor if the cursor moves directionally with the left-hand forces, whereas the right hand primarily acts if it moves with the opposing right-hand forces. In neurophysiological (electromyography, transcranial magnetic brain stimulation) and functional magnetic resonance brain imaging experiments we demonstrate that changes in hand assignment parallels a midline shift of lateralized activity in distal hand muscles, corticospinal pathways, and primary sensorimotor and cerebellar cortical areas. We conclude that the two hands can readily exchange roles as dominant actor in bimanual tasks. Spatial relationships between hand forces and goal motions determine hand assignments rather than habitual handedness. Finally, flexible role assignment of the hands is manifest at multiple levels of the motor system, from cortical regions all the way down to particular muscles.

Brain↗

Eye-hand coordination during learning of a novel visuomotor task.

We investigated how gaze behavior and eye-hand coordination change when subjects learned a challenging visuomotor task that required acquisition of a novel mapping between bimanual actions and their visual sensory consequences. By applying isometric forces and torques to a rigid tool held freely between the two hands, subjects learned to control a cursor on a computer screen to hit successively displayed targets as quickly as possible. The learning occurred in stages that could be distinguished by changes in performance (target-hit rate) as well as by gaze behavior and eye-hand coordination. In a first exploratory stage, the hit rate was consistently low, the cursor position varied widely, and gaze typically pursued the cursor. In a second skill acquisition stage, the hit rate improved rapidly, and gaze fixations began to mark predictively desired cursor positions, indicating that subjects started to program spatially congruent eye and hand motor commands. In a third skill refinement stage, performance continued to improve gradually, and gaze shifted directly toward the target. We suggest that during the exploratory stage, the learner attempts to establish basic mapping rules between manual actions and eye-movement commands. In this process, subjects may establish correlations between hand motor commands and their visual sensory consequences, primarily in fovea-anchored, gaze-centered coordinates, and correlations between recent hand motor commands and eye motor commands. The established mapping rules are then implemented and refined in the skill acquisition and refinement stages.

Adult↗

First spikes in ensembles of human tactile afferents code complex spatial fingertip events.

It is generally assumed that primary sensory neurons transmit information by their firing rates. However, during natural object manipulations, tactile information from the fingertips is used faster than can be readily explained by rate codes. Here we show that the relative timing of the first impulses elicited in individual units of ensembles of afferents reliably conveys information about the direction of fingertip force and the shape of the surface contacting the fingertip. The sequence in which different afferents initially discharge in response to mechanical fingertip events provides information about these events faster than the fastest possible rate code and fast enough to account for the use of tactile signals in natural manipulation.

Action Potentials↗

Action plans used in action observation.

How do we understand the actions of others? According to the direct matching hypothesis, action understanding results from a mechanism that maps an observed action onto motor representations of that action. Although supported by neurophysiological and brain-imaging studies, direct evidence for this hypothesis is sparse. In visually guided actions, task-specific proactive eye movements are crucial for planning and control. Because the eyes are free to move when observing such actions, the direct matching hypothesis predicts that subjects should produce eye movements similar to those produced when they perform the tasks. If an observer analyses action through purely visual means, however, eye movements will be linked reactively to the observed action. Here we show that when subjects observe a block stacking task, the coordination between their gaze and the actor's hand is predictive, rather than reactive, and is highly similar to the gaze-hand coordination when they perform the task themselves. These results indicate that during action observation subjects implement eye motor programs directed by motor representations of manual actions and thus provide strong evidence for the direct matching hypothesis.

Adult↗

Loads applied tangential to a fingertip during an object restraint task can trigger short-latency as well as long-latency EMG responses in hand muscles.

Electrical stimulation of the digital nerves can cause short- and long-latency increases in electromyographic activity (EMG) of the hand muscles, but mechanical stimulation of primarily tactile afferents in the digits generally evokes only a long-latency increase in EMG. To examine whether such stimuli can elicit short-latency reflex responses, we recorded EMG over the first dorsal interosseous muscle when subjects (n=13) used the tip of the right index finger to restrain a horizontally oriented plate from moving when very brisk tangential forces were applied in the distal direction. The plate was subjected to ramp-and-hold pulling loads at two intensities (a 1-N load applied at 32 N/s or a 2-N load applied at 64 N/s) at times unpredictable to the subjects (mean interval 2 s; trial duration 500 ms). The contact surface of the manipulandum was covered with rayon--a slippery material. For each load, EMG was averaged for 128 consecutive trials with reference to the ramp onset. In all subjects, an automatic increase in grip force was triggered by the loads applied at 32 N/s; the mean onset latency of the EMG response was 59.8 +/- 0.9 (mean +/- SE) ms. In seven subjects (54%) this long-latency response was preceded by a weak short-latency excitation at 34.6 +/- 2.9 ms. With the loads applied at 64 N/s, the long-latency response occurred slightly earlier (58.9 +/- 1.7 ms) and, with one exception, all subjects generated a short-latency EMG response (34.9 +/- 1.3 ms). Despite the higher background grip force that subjects adopted during the stronger loads (4.9 +/- 0.3 N vs 2.5 +/- 0.2 N), the incidence of slips was higher--the manipulandum escaped from the grasp in 37 +/- 5% of trials with the 64 N/s ramps, but in only 18 +/- 4% with the 32-N/s ramps. The deformation of the fingertip caused by the tangential load, rather than incipient or overt slips, triggered the short-latency responses because such responses occurred even when the finger pad was fixed to the manipulandum with double-sided adhesive tape so that no slips occurred.

Adult↗

Prediction precedes control in motor learning.

Skilled motor behavior relies on the brain learning both to control the body and predict the consequences of this control. Prediction turns motor commands into expected sensory consequences, whereas control turns desired consequences into motor commands. To capture this symmetry, the neural processes underlying prediction and control are termed the forward and inverse internal models, respectively. Here, we investigate how these two fundamental processes are related during motor learning. We used an object manipulation task in which subjects learned to move a hand-held object with novel dynamic properties along a prescribed path. We independently and simultaneously measured subjects' ability to control their actions and to predict their consequences. We found different time courses for predictor and controller learning, with prediction being learned far more rapidly than control. In early stages of manipulating the object, subjects could predict the consequences of their actions, as measured by the grip force they used to grasp the object, but could not generate appropriate actions for control, as measured by their hand trajectory. As predicted by several recent theoretical models of sensorimotor control, our results indicate that people can learn to predict the consequences of their actions before they can learn to control their actions.

Biophysical Phenomena↗

Influence of object shape on responses of human tactile afferents under conditions characteristic of manipulation.

Most objects that we grasp, lift and further manipulate are curved, with curvatures of the same order of magnitude as those of the fingertips. Tactile information pertaining to such 'gross' geometrical features of objects are used in the automatic control of fingertip actions. We analyzed responses from 172 human tactile afferents distributed over the entire terminal phalanx when spherically shaped surfaces were applied to a standard site on the fingertip; the curvatures and force magnitudes and directions used were representative of everyday manipulations. Nearly all SA-I, SA-II and FA-I afferents responded, and for more than 80% of these afferents the response intensity was correlated with curvature. The correlation was positive for approximately half the afferents and negative for the other half, resulting in a curvature contrast signal within the populations of tactile afferents; afferents terminating at the sides and end of the fingertip tended to show negative correlations. For nearly all afferents, curvature and force direction had interactive effects. Changing the direction of force affected an afferent's sensitivity to curvature and vice versa. We conclude that recognition of such shapes takes advantage of signals originating from tactile afferents distributed over the entire terminal phalanx, and that both the direction of fingertip forces and the curvatures of objects contacted during natural manipulations influence the afferents' responses. Consequently, if humans are able to perceive independently curvature and force direction from signals in tactile afferents, then the CNS must possess mechanisms that disentangle interactions between these and other parameters of stimuli on the fingertips.

Adult↗

Evidence for the involvement of the posterior parietal cortex in coordination of fingertip forces for grasp stability in manipulation.

Grasp stability during object manipulation is achieved by the grip forces applied normal to the grasped surfaces increasing and decreasing in phase with increases and decreases of destabilizing load forces applied tangential to the grasped surfaces. This force coordination requires that the CNS anticipates the grip forces that match the requirements imposed by the self-generated load forces. Here, we use functional MRI (fMRI) to study neural correlates of the grip-load force coordination in a grip-load force task in which six healthy humans attempted to lift an immovable test object held between the tips of the right index finger and thumb. The recorded brain activity was compared with the brain activity obtained in two control tasks in which the same pair of digits generated forces with similar time courses and magnitudes; i.e., a grip force task where the subjects only pinched the object and did not apply load forces, and a load force task, in which the subjects applied vertical forces to the object without generating grip forces. Thus neither the load force task nor the grip force task involved coordinated grip-load forces, but together they involved the same grip force and load force output. We found that the grip-load force task was specifically associated with activation of a section of the right intraparietal cortex, which is the first evidence for involvement of the posterior parietal cortex in the sensorimotor control of coordinated grip and load forces in manipulation. We suggest that this area might represents a node in the network of cortical and subcortical regions that implement anticipatory control of fingertip forces for grasp stability.

Adult↗

Orofacial mechanoreceptors in humans: encoding characteristics and responses during natural orofacial behaviors.

We used microneurography to characterize stimulus-encoding properties of low-threshold mechanoreceptive afferents in human orofacial tissues. Signals were recorded from single afferents in the infraorbital, lingual and inferior alveolar nerves while localized, controlled, mechanical stimuli were delivered to the facial skin, lips, oral mucosa and teeth. We likewise analyzed activity in these afferents during orofacial behaviors such as speech, chewing and biting. The afferents in the soft tissues functionally resemble four types described in the human hand: hair follicle afferents, slowly adapting (SA) type I and type II afferents and fast adapting (FA) type I afferents. Afferents in the facial skin, lips and buccal mucosa respond not only to contact with environmental objects, but also to contact between the lips, changes in air pressure generated for speech sounds, and to facial skin and mucosa deformations that accompany lip and jaw movements associated with chewing and swallowing. Hence, in addition to exteroceptive information, these afferents provide proprioceptive information. In contrast, afferents terminating superficially in the tongue do not signal proprioceptive information about tongue movements in this manner. They only respond when the receptive field is brought into contact with other intraoral structures or objects, e.g. the teeth or food. All human periodontal afferents adapt slowly to maintained tooth loads. Populations of periodontal afferents encode information about both which teeth are loaded and the direction of forces applied to individual teeth. Most afferents exhibit a markedly curved relationship between discharge rate and force amplitude, featuring the highest sensitivity to changes in tooth load at low forces (below 1 N). Accordingly, periodontal afferents efficiently encode tooth load when subjects first contact, hold, and gently manipulate food by the teeth. In contrast, only a minority of the afferents encodes the rapid and strong force increase generated when biting through food. We conclude, that humans use periodontal afferent signals to control jaw actions associated with intraoral manipulation of food rather than exertion of jaw power actions.

Behavior↗

Predictions specify reactive control of individual digits in manipulation.

When humans proactively manipulate objects, the applied fingertip forces primarily depend on feedforward, predictive neural control mechanisms that depend on internal representations of the physical properties of the objects. Here we investigate whether predictions of object properties also control fingertip forces that subjects generate reactively. We analyzed fingertip forces reactively supporting grasp stability in a restraining task that engaged two fingers. Each finger contacted a plate mounted on a separate torque motor, and, at unpredictable times, both plates were loaded simultaneously with forces tangential to the plates or just one of the plates was loaded. Thus, the apparatus acted as though the plates were mechanically linked or as though they were two independent objects. In different test series, each with a predominant behavior of the apparatus and with interspersed catch trials, we showed that the reactive responses clearly reflected the predominant behavior of the apparatus. Whether subject performed the task with one hand or bimanually, appropriate reactive fingertip forces developed when predominantly both contact plates were loaded or just one of the plates was loaded. When a finger was unexpectedly loaded during a catch trial, a weak initial reactive response was triggered, but the effective force development was delayed by approximately 100 msec. We conclude that the predicted physical properties of an object not only control fingertip forces during proactive but also in reactive manipulative tasks. Specifically, the automatic reactive responses reflect predictions at the level of individual digits as to the mechanical linkage of items contacted by the fingertips in manipulation.

Adult↗

Incidence of F waves in single human thenar motor units.

F-wave generation, axon conduction velocities, and contractile properties were compared in 44 healthy individual human thenar motor units. Force and muscle action potentials were recorded when single motor axons were stimulated intraneurally about 10 cm proximal to the elbow. Each stimulus usually evoked only one electromyographic (EMG) potential. However, in seven units (16%), a single stimulus elicited an F wave in response to 1.7 +/- 1.6% (mean +/- SD) of the stimuli applied. Axon conduction velocity proximal to the site of stimulation was faster than distal conduction velocity (72.7 +/- 8.0 m/s versus 64.2 +/- 10.5 m/s). Distal conduction velocities, twitch forces, and contraction times were similar for units that did and did not generate F waves. Thus, no obvious subset of thenar motor units generated F waves. These results provide valuable baseline information on F waves that can be used to assess changes in axon conduction, motor unit contractile properties, and motoneuron excitability in disease.

Electric Stimulation↗

Dynamic use of tactile afferent signals in control of dexterous manipulation.

During object manipulation, humans select and activate neural action programs acquired during ontogenetic development. A basic issue in understanding the control of dexterous manipulation is to learn how people use sensory information to adapt the output of these neural programs such that the fingertip actions matches the requirements imposed by the physical properties of the manipulated object, e.g., weight (mass), slipperiness, shape, and mass distribution. Although visually based identification processes contribute to predictions of required fingertip actions, the digital tactile sensors provide critical information for the control of fingertip forces. The present account deals with the tactile afferent signals from the digits during manipulation and focuses on some specific issues that the neural controller has to deal with to make use of tactile information.

Fingers↗

Engagement of gaze in capturing targets for future sequential manual actions.

We investigated the role of saccadic gaze fixations in encoding target locations for planning a future manual task consisting of a sequence of discrete target-oriented actions. We hypothesized that fixations of the individual targets are necessary for accurate encoding of target locations and that there is a transfer of sequence information from visual encoding to manual recall. Subjects viewed four targets presented at random positions on a screen. After various delays following target extinction, the subjects marked the remembered target locations on the screen with the tip of a hand-held stick. When the targets were presented simultaneously among distracting elements, the overall accuracy of marking increased with presentation time and total number of targets fixated because the subjects had to serially fixate the individual targets to locate them. Without distractors, the marking accuracy was similarly high regardless of duration of target presentation (0.25-8 s) and number of targets fixated; it was comparable to that with distractors when all four targets had been fixated. This indicates parallel encoding of target locations largely based on peripheral vision. Location memory was stable in these tasks over the delay periods investigated (0.5-8 s). With parallel encoding there was a "shrinkage" in the visuomotor transformation, i.e., the distances between the markings were systematically smaller than the corresponding inter-target distances. When the targets were presented sequentially without distractors, marking accuracy improved with the total number of targets fixated and shrinkage in the visuomotor transformation occurred only with parallel encoding, i.e., when subjects did not fixate the targets. In all experimental conditions for trials in which targets were fixated during encoding, there was little correspondence between the marking sequence and the sequence in which the targets were fixated. We conclude that subjects benefit from fixating targets for subsequent target-oriented manual actions when the targets are presented among distractors and when presented sequentially; when distinct targets are presented simultaneously against a blank background, they are efficiently encoded in parallel largely by peripheral vision.

Adult↗