Sensorimotor Memory Research Articles

Effects of Carpal Tunnel Syndrome on Adaptation of Multi-Digit Forces to Object Weight for Whole-Hand Manipulation

The delicate tuning of digit forces to object properties can be disrupted by a number of neurological and musculoskeletal diseases. One such condition is Carpal Tunnel Syndrome (CTS), a compression neuropathy of the median nerve that causes sensory and motor deficits in a subset of digits in the hand. Whereas the effects of CTS on median nerve physiology are well understood, the extent to which it affects whole-hand manipulation remains to be addressed. CTS affects only the lateral three and a half digits, which raises the question of how the central nervous system integrates sensory feedback from affected and unaffected digits to plan and execute whole-hand object manipulation. We addressed this question by asking CTS patients and healthy controls to grasp, lift, and hold a grip device (445, 545, or 745 g) for several consecutive trials. We found that CTS patients were able to successfully adapt grip force to object weight. However, multi-digit force coordination in patients was characterized by lower discrimination of force modulation to lighter object weights, higher across-trial digit force variability, the consistent use of excessively large digit forces across consecutive trials, and a lower ability to minimize net moments on the object. Importantly, the mechanical requirement of attaining equilibrium of forces and torques caused CTS patients to exert excessive forces at both CTS-affected digits and digits with intact sensorimotor capabilities. These findings suggest that CTS-induced deficits in tactile sensitivity interfere with the formation of accurate sensorimotor memories of previous manipulations. Consequently, CTS patients use compensatory strategies to maximize grasp stability at the expense of exerting consistently larger multi-digit forces than controls. These behavioral deficits might be particularly detrimental for tasks that require fine regulation of fingertip forces for manipulating light or fragile objects.

Remembering forward: Neural correlates of memory and prediction in human motor adaptation

We used functional MR imaging (FMRI), a robotic manipulandum and systems identification techniques to examine neural correlates of predictive compensation for spring-like loads during goal-directed wrist movements in neurologically-intact humans. Although load changed unpredictably from one trial to the next, subjects nevertheless used sensorimotor memories from recent movements to predict and compensate upcoming loads. Prediction enabled subjects to adapt performance so that the task was accomplished with minimum effort. Population analyses of functional images revealed a distributed, bilateral network of cortical and subcortical activity supporting predictive load compensation during visual target capture. Cortical regions--including prefrontal, parietal and hippocampal cortices--exhibited trial-by-trial fluctuations in BOLD signal consistent with the storage and recall of sensorimotor memories or "states" important for spatial working memory. Bilateral activations in associative regions of the striatum demonstrated temporal correlation with the magnitude of kinematic performance error (a signal that could drive reward-optimizing reinforcement learning and the prospective scaling of previously learned motor programs). BOLD signal correlations with load prediction were observed in the cerebellar cortex and red nuclei (consistent with the idea that these structures generate adaptive fusimotor signals facilitating cancelation of expected proprioceptive feedback, as required for conditional feedback adjustments to ongoing motor commands and feedback error learning). Analysis of single subject images revealed that predictive activity was at least as likely to be observed in more than one of these neural systems as in just one. We conclude therefore that motor adaptation is mediated by predictive compensations supported by multiple, distributed, cortical and subcortical structures.

Writing strengthens orthography and alphabetic-coding strengthens phonology in learning to read Chinese.

Learning to write words may strengthen orthographic representations and thus support word-specific recognition processes. This hypothesis applies especially to Chinese because its writing system encourages character-specific recognition that depends on accurate representation of orthographic form. We report 2 studies that test this hypothesis in adult learners of Chinese. In those studies, the researchers 1st compared the effects of an online writing tutor that included character handwriting with an instructional tutor that included reading only. The writing condition led to better performance on word recognition and on character-meaning links but not on the character-phonology link. In the 2nd experiment, we added an alphabetic (Pinyin) typing tutor to strengthen the phonology link and to control for manual motor activity during instruction. This experiment replicated the effects of writing on word recognition and character-meaning links, whereas alphabetic (Pinyin) typing supported only phonological representations and the character-phonology link. Theoretically, the studies suggest constituent-specific effects: writing on orthography and alphabetic coding on phonology. We suggest the mechanism for the writing effect is the refinement of visual-spatial information needed for character recognition and the addition of a sensory-motor memory that accompanies writing. The practical implication is that an integration of character handwriting and Pinyin typing promotes learning to read Chinese in a second language learning context.

Theta-Burst Stimulation of the Cerebellum Interferes with Internal Representations of Sensory-Motor Information Related to Eye Movements in Humans

Continuous theta-burst stimulation (cTBS) applied over the cerebellum exerts long-lasting effects by modulating long-term synaptic plasticity, which is thought to be the basis of learning and behavioral adaptation. To investigate the impact of cTBS over the cerebellum on short-term sensory-motor memory, we recorded in two groups of eight healthy subject each the visually guided saccades (VGSs), the memory-guided saccades (MGSs), and the multiple memory-guided saccades (MMGSs), before and after cTBS (cTBS group) or simulated cTBS (control group). In the cTBS group, cTBS determined hypometria of contralateral centrifugal VGSs and worsened the accuracy of MMGS bilaterally. In the control group, no significant differences were found between the two recording sessions. These results indicate that cTBS over the cerebellum causes eye movement effects that last longer than the stimulus duration. The VGS contralateral hypometria suggested that we eventually inhibited the fastigial nucleus on the stimulated side. MMGSs in normal subjects have a better final accuracy with respect to MGSs. Such improvement is due to the availability in MMGSs of the efference copy of the initial reflexive saccade directed toward the same peripheral target, which provides a sensory-motor information that is memorized and then used to improve the accuracy of the subsequent volitional memory-guided saccade. Thus, we hypothesize that cTBS disrupted the capability of the cerebellum to make an internal representation of the memorized sensory-motor information to be used after a short interval for forward control of saccades.

The Influence of Exposure Amount on the Persistence of Short-Term, Haptically Acquired Sensorimotor Memorial Representations

This study investigates the influence that the amount of exposure has on the persistence of sensorimotor memories. Participants acquired memories of an unexpectedly heavy object in one of four groups that varied in the number lifts of the object they each performed. All participants followed this acquisition period with retention lifts immediately and after 2-second and 10-second intervals, as well as after 15 minutes and 24 hours. Grasp force profiles were evaluated for the maintenance of memory-dependent adaptations. A lack of any group effects indicates that the quantity of exposure offers the sensorimotor memory system no temporal advantage in the maintenance of short-term representations. The results are discussed in light of the possibility that, within a short time frame, only the information from the preceding lift has functional relevance to the current lift.

Limited persistence of the sensorimotor memory when transferred across prehension tasks

A recent study has shown that the sensorimotor memory for the fingertip forces used to grasp and lift an object can be shared across two prehension tasks. However, the persistence (or decay) of these memory resources is not known. Reports of within-task sensorimotor memory indicate persistence of lifting forces, with evidence for reduced persistence of grip forces. Here we investigated the temporal dynamics of the transfer of memory related to vertical lifting forces across prehension tasks. Young adult participants in two separate experimental groups first held the object placed on their palm and ‘hefted’ it (moved it up and down) followed by lifting the object using a precision grip (thumb-finger) with the dominant hand after a delay of 10 s, or 20 min. The Control group lifted the object with the dominant hand using a precision grip and then did so again 20 min later. The Control group used higher load force rates (LFR) for their first lift compared to subsequent lifts, both before and after the 20-min delay. This suggests that the Control group initially overestimated the weight of the object, corrected their LFRs, and then was able to retain this corrected force scaling after the 20-min delay. The Experimental 10-second delay group accurately scaled their LFRs upon their first lift, indicating that they obtained an accurate memory for LFR scaling during hefting, and transferred it to the lift task. In contrast, the Experimental 20-minute delay group was unable to scale their LFRs upon their first lift, as indicated by high LFRs that were no different than those of the Control group. Thus, the memory related to the production of LFR remained stable over 20 min when obtained from the same task, while that obtained from a different task decayed completely within 20 min. This decay may indicate weakened sensorimotor memories related to prehension forces due to its dependence not only on the memory for object mechanical properties, but also on sensory signals generated during the prehension act, along with strong visual prior estimates of a size-weight relationship.

Neurobehavioral changes in mice offspring induced by prenatal exposure to acute toxicity of sodium selenite

Selenium is an essential element with a narrow margin between beneficial and toxic effects. This study was aimed to determine the neurobehavioral changes resulted from the prenatal exposure of mice to high doses of sodium selenite during fetal and early postnatal development. Atomic absorption for monitoring the placental transfer of selenium to offspring was employed. The developmental observations as well as the behavioral tests, such as sensory motor reflexes, and learning and memory test in automatic reflex conditioner (shuttle box) (active avoidance responses) were applied. Adult mice was assigned into three groups: the first group was remained as a control group given phosphate buffered saline; the second and the third groups were orally administrated sodium selenite at doses of 1 mg/kg and 4 mg/kg of the diet, respectively started from the 7th day to the end of the gestation period. Appearance of body hair and opening of eyes of the pups from treated mothers were delayed in a dose-dependent manner. The body weight gain came significantly lower than those of the control especially at the higher dose. Selenite also inhibited the sensory motor reflexes in all elements of acts and postures in a dose dependent manner. The active avoidance training-test indicated that selenite exposure was associated with learning impairment. Acetylcholine recorded a significant decrease in almost all the period of this study. By using atomic absorption, we found a significant high concentration of selenium in the brain, liver and kidney until the 40th postnatal day, indicating active transfer of selenium from mothers to embryos.

Anticipatory Planning and Control of Grasp Positions and Forces for Dexterous Two-Digit Manipulation

Dexterous object manipulation requires anticipatory control of digit positions and forces. Despite extensive studies on sensorimotor learning of digit forces, how humans learn to coordinate digit positions and forces has never been addressed. Furthermore, the functional role of anticipatory modulation of digit placement to object properties remains to be investigated. We addressed these questions by asking human subjects (12 females, 12 males) to grasp and lift an inverted T-shaped object using precision grip at constrained or self-chosen locations. The task requirement was to minimize object roll during lift. When digit position was not constrained, subjects could have implemented many equally valid digit position-force coordination patterns. However, choice of digit placement might also have resulted in large trial-to-trial variability of digit position, hence challenging the extent to which the CNS could have relied on sensorimotor memories for anticipatory control of digit forces. We hypothesized that subjects would modulate digit placement for optimal force distribution and digit forces as a function of variable digit positions. All subjects learned to minimize object roll within the first three trials, and the unconstrained device was associated with significantly smaller grip forces but larger variability of digit positions. Importantly, however, digit load force modulation compensated for position variability, thus ensuring consistent object roll minimization on each trial. This indicates that subjects learned object manipulation by integrating sensorimotor memories with sensory feedback about digit positions. These results are discussed in the context of motor equivalence and sensorimotor integration of grasp kinematics and kinetics.

Diffuse traumatic axonal injury induces sensorimotor deficit, memory loss and hippocampal axonal hyperexcitability

Diffuse traumatic axonal injury induces sensorimotor deficit, memory loss and hippocampal axonal hyperexcitability

Erasing sensorimotor memories via PKMzeta inhibition.

Sensorimotor cortex has a role in procedural learning. Previous studies suggested that this learning is subserved by long-term potentiation (LTP), which is in turn maintained by the persistently active kinase, protein kinase Mzeta (PKMζ). Whereas the role of PKMζ in animal models of declarative knowledge is established, its effect on procedural knowledge is not well understood. Here we show that PKMζ inhibition, via injection of zeta inhibitory peptide (ZIP) into the rat sensorimotor cortex, disrupts sensorimotor memories for a skilled reaching task even after several weeks of training. The rate of relearning the task after the memory disruption by ZIP was indistinguishable from the rate of initial learning, suggesting no significant savings after the memory loss. These results indicate a shared molecular mechanism of storage for declarative and procedural forms of memory.

Information about the Weight of Grasped Objects from Vision and Internal Models Interacts within the Primary Motor Cortex

When grasping and lifting different objects, visual cues and previously acquired knowledge enable us to prepare the upcoming grasp by scaling the fingertip forces according to the actual weight of the object. However, when no visual information is available, the weight of the object has to be predicted based on information learned from previous grasps. Here, we investigated how changes in corticospinal excitability (CSE) and grip force scaling depend on the presence of visual cues and the weight of previously lifted objects. CSE was assessed by delivering transcranial magnetic stimulation (TMS) at different times before grasp of the object. In conditions in which visual information was not provided, the size of motor evoked potentials (MEP) was larger when the object lifted was preceded by a heavy relative to a light object. Interestingly, the previous lift also affected MEP amplitude when visual cues about object weight were available but only in the period immediately after object presentation (50 ms); this effect had already declined for TMS delivered 150 ms after presentation. In a second experiment, we demonstrated that these CSE changes are used by the motor system to scale grip force. This suggests that the corticospinal system stores a "sensorimotor memory" of the grasp of different objects and relies on this memory when no visual cues are present. Moreover, visual information about weight interacts with this stored representation and allows the corticospinal system to switch rapidly to a different model of predictive grasp control.

On the Content of Sensorimotor Representations After Actual and Motor Imagery Practice

We examined the similarities between actual and motor imagery practice with regard to the development of sensorimotor representations. Participants had to reproduce knee joint positions (15 or 150 trials) in visuo-proprioceptive or proprioceptive conditions (Experiment 1) or in visual, proprioceptive or visuo-proprioceptive imagery conditions (Experiment 2), before being transferred in a proprioceptive condition. A familiarization session in a proprioceptive condition was performed before imagery practice only (Experiment 2). Results showed that the effect of vision withdrawal varied according to actual or motor imagery practice: performance accuracy in transfer decreased after actual visuo-proprioceptive practice while it increased after visuo-proprioceptive imagery practice. These results suggest that different movement representations can be developed following actual or imagery practice. They also suggest that information from previous experience could be stored in a sensorimotor memory and could be fundamental for the efficiency of motor imagery practice.

Manipulation After Object Rotation Reveals Independent Sensorimotor Memory Representations of Digit Positions and Forces

Planning of object manipulations is dependent on the ability to generate, store, and retrieve sensorimotor memories of previous actions associated with grasped objects. However, the sensorimotor memory representations linking object properties to the planning of grasp are not well understood. Here we use an object rotation task to gain insight into the mechanisms underlying the nature of these sensorimotor memories. We asked subjects to grasp a grip device with an asymmetrical center of mass (CM) anywhere on its vertical surfaces and lift it while minimizing object roll. After subjects learned to minimize object roll by generating a compensatory moment, they were asked to rotate the object 180 degrees about a vertical axis and lift it again. The rotation resulted in changing the direction of external moment opposite to that experienced during the prerotation block. Anticipatory grasp control was quantified by measuring the compensatory moment generated at object lift onset by thumb and index finger forces through their respective application points. On the first postrotation trial, subjects failed to generate a compensatory moment to counter the external moment caused by the new CM location, thus resulting in a large object roll. Nevertheless, after several object rotations subjects reduced object roll on the initial postrotation trials by anticipating the new CM location through the modulation of digit placement but not tangential forces. The differential improvement in modulating these two variables supports the notion of independent memory representations of kinematics and kinetics and is discussed in relation to neural mechanisms underlying visuomotor transformations.

On the role of imagery modalities on motor learning

In the present study, we examine specifically how the sensory conditions available during physical practice of a task might influence the subsequent use of motor imagery. First, as a pre-test, participants had to physically reproduce knee joint positions with or without vision. Second, they practised motor imagery (15 and 150 trials) with visual, kinaesthetic or visuo-kinaesthetic imagery. A control group with no imagery was included. Post-tests were then performed 10 min and 24 h after each imagery session in a sensory condition similar to that used in the pre-test. Results showed that efficient motor imagery instructions have to take account of the sensory information available during physical experience of the task: kinaesthetic or visuo-kinaesthetic imagery in a no-vision condition, and visual imagery or, to a lesser extent, visuo-kinaesthetic imagery in a vision condition. Discussion focuses on the role of sensory motor memory on motor prediction to simulate a specific movement, and on the similarities between physical and mental practice in the development of sensory-specific movement representation.

Anticipatory Modulation of Digit Placement for Grasp Control Is Affected by Parkinson's Disease

BackgroundSuccessful object manipulation relies on the ability to form and retrieve sensorimotor memories of digit forces and positions used in previous object lifts. Past studies of patients affected by Parkinson's disease (PD) have revealed that the basal ganglia play a crucial role in the acquisition and/or retrieval of sensorimotor memories for grasp control. Whereas it is known that PD impairs anticipatory control of digit forces during grasp, learning deficits associated with the planning of digit placement have yet to be explored. This question is motivated by recent work in healthy subjects revealing that anticipatory control of digit placement plays a crucial role for successful manipulation.Methodology/Principal FindingsWe asked ten PD patients off medication and ten age-matched controls to reach, grasp and lift an object whose center of mass (CM) was on the left, right or center. The only task requirement was to minimize object roll during lift. The CM remained the same across consecutive trials (blocked condition) or was altered from trial to trial (random condition). We hypothesized that impairment of the basal ganglia-thalamo-cortical circuits in PD patients would reduce their ability to anticipate digit placement appropriate to the CM location. Consequently, we predicted that PD patients would exhibit similar digit placement in the blocked vs. random conditions and produce larger peak object rolls than that of control subjects. In the blocked condition, PD patients exhibited significantly weaker modulation of fingertip contact points to CM location and larger object roll than controls (p<0.05 and p<0.01, respectively). Nevertheless, both controls and PD patients minimized object roll more in the blocked than in the random condition (p<0.01).Conclusions/SignificanceOur findings indicate that, even though PD patients may have a residual ability of anticipatory control of digit contact points and forces, they fail to implement a motor plan with the same degree of effectiveness as controls. We conclude that intact basal ganglia-thalamo-cortical circuits are necessary for successful sensorimotor learning of both grasp kinematics and kinetics required for dexterous hand-object interactions.

Motor adaptation and manual transfer: Insight into the persistent nature of sensorimotor representations

It is well known that sensorimotor memories are built and updated through experience with objects. These representations are useful to anticipatory and feedforward control processes that preset grip and load forces during lifting. When individuals lift objects with qualities that are not congruent with their memory-derived expectations, feedback processes adjust motor plans to achieve successful lifts and contribute to the updating of the stored representations. The two experiments presented examine motor adaptation to an illusory size–weight lifting task, and the transfer of this motor adaptation to the unexposed hand. In Experiment 1, performers acquired motor adaptation with their right hand and transfer was measured on their left hand. In Experiment 2, adaptation was acquired with the left hand and transfer was measured on the right hand. In order to investigate the persistence of sensorimotor memories, these experiments measure adaptation, retention, and transfer after 15 min and 24 h delay periods. Both experiments confirm that experience with objects leads to adaptation of force scaling processes, that these adaptations transcend effector and are persistent. The results are discussed in terms favouring interpretations that describe motor adaptations to illusion as being centrally available.

Intermanual transfer of sensorimotor memory for grip force when lifting objects: The role of wrist angulation

To investigate the mechanisms underlying the intermanual transfer of sensorimotor memory when lifting an object. Twenty healthy subjects grasped and lifted an object with constant mechanical properties with the right hand (RH) first and then with the left hand (LH). Ten of the subjects lifted the object with the RH in a regular wrist angulation (WA), followed by lifts with the LH in a regular WA. The remaining 10 subjects lifted the object with the RH in a hyper-flexed WA, followed by lifts with the LH in a regular WA. Subjects generated greater peak grip force (GF) rates, grip and lift forces when lifting the object with the wrist in a regular WA compared to lifts with the wrist in hyper-flexion. Importantly, subjects transferred the predictive scaling of GF from the RH to the LH, regardless of the WA. Biomechanical properties of the object do not seem to be used by the CNS as a first line information to evaluate GF when handling an object or transferring information about the grasp to the opposite hemisphere. The predictive scaling of GF rather reflects an internal sense of effort than an internal representation of the mechanical object properties.

Sensorimotor memory of object weight distribution during multidigit grasp

We studied the ability to transfer three-digit force sharing patterns learned through consecutive lifts of an object with an asymmetric center of mass (CM). After several object lifts, we asked subjects to rotate and translate the object to the contralateral hand and perform one additional lift. This task was performed under two weight conditions (550 and 950 g) to determine the extent to which subjects would be able to transfer weight and CM information. Learning transfer was quantified by measuring the extent to which force sharing patterns and peak object roll on the first post-translation trial resembled those measured on the pre-translation trial with the same CM. We found that the overall gain of fingertip forces was transferred following object rotation, but that the scaling of individual digit forces was specific to the learned digit-object configuration, and thus was not transferred following rotation. As a result, on the first post-translation trial there was a significantly larger object roll following object lift-off than on the pre-translation trial. This suggests that sensorimotor memories for weight, requiring scaling of fingertip force gain, may differ from memories for mass distribution.

Collision error avoidance: influence of proportion congruency and sensorimotor memory on open-loop grasp control

Grasping behaviour involves the integration of current and historical knowledge about an object, a process that can be influenced by sensory uncertainty. In the present study, participants simultaneously interacted with a visual cue and a haptic cue before reaching to grasp a target object. The visual cue was either congruent (equal in size to haptic cue and target) or incongruent (larger than haptic cue and target). To enhance sensory uncertainty, we manipulated the proportion of congruent trials to be either 80 or 20%. We compared grasp kinematics and forces between congruent and incongruent trials and between the 20 and 80% proportion congruency groups. We also studied the effects of trial history by comparing the performance of congruent and incongruent trials preceded by either the same or opposite trial type. Proportion congruency did not affect temporal kinematics but did affect maximum grip aperture (MGA) as the 80% proportion congruency group used a greater MGA, regardless of trial type. For grasping forces, an interaction effect showed that the 20% proportion congruency group used a greater peak load force on congruent trials. Incongruent trials that followed congruent trials had decreased movement time, increased MGA and increased grasping forces, relative to those that followed incongruent trials. We interpret the data to suggest that the grasp control system integrates multisensory information using flexible, yet specific criteria regarding task constraints. The prevention of collision error (i.e., an inadequate MGA when contacting the target) may be one guiding principle in the control process.

Anticipatory Control of Grasping: Independence of Sensorimotor Memories for Kinematics and Kinetics

We have recently provided evidence for anticipatory grasp control mechanisms in the kinematic domain by showing that subjects modulate digit placement on an object based on its center of mass (CM) when it can be anticipated (Lukos et al., 2007). This behavior relied on sensorimotor memories about digit contact points and forces required for optimal manipulation. We found that accurate sensorimotor memories depended on the acquisition of implicit knowledge about object properties associated with repeated manipulations of the same object. Whereas implicit knowledge of object properties is essential for anticipatory grasp control, the extent to which subjects can use explicit knowledge to accurately scale digit forces in an anticipatory manner is controversial. Additionally, it is not known whether subjects are able to use explicit knowledge of object properties for anticipatory control of contact points. We addressed this question by asking subjects to grasp and lift an object while providing explicit knowledge of object CM location as visual or verbal cues. Contact point modulation and object roll, a measure of anticipatory force control, were assessed using blocked and random CM presentations. We found that explicit knowledge of object CM enabled subjects to modulate contact points. In contrast, subjects could not minimize object roll in the random condition to the same extent as in the blocked when provided with a verbal or visual cue. These findings point to a dissociation in the effect of explicit knowledge of object properties on grasp kinematics versus kinetics, thus suggesting independent anticipatory processes for grasping.