Object weight can be rapidly predicted, with low cognitive load, by exploiting learned associations between the weights and locations of objects.

Weight prediction is critical for dexterous object manipulation. Previous work has focused on lifting objects presented in isolation and has examined how the visual appearance of an object is used to predict its weight. Here we tested the novel hypothesis that when interacting with multiple objects, as is common in everyday tasks, people exploit the locations of objects to directly predict their weights, bypassing slower and more demanding processing of visual properties to predict weight. Using a three-dimensional robotic and virtual reality system, we developed a task in which participants were presented with a set of objects. In each trial a randomly chosen object translated onto the participant's hand and they had to anticipate the object's weight by generating an equivalent upward force. Across conditions we could control whether the visual appearance and/or location of the objects were informative as to their weight. Using this task, and a set of analogous web-based experiments, we show that when location information was predictive of the objects' weights participants used this information to achieve faster prediction than observed when prediction is based on visual appearance. We suggest that by "caching" associations between locations and weights, the sensorimotor system can speed prediction while also lowering working memory demands involved in predicting weight from object visual properties.NEW & NOTEWORTHY We use a novel object support task using a three-dimensional robotic interface and virtual reality system to provide evidence that the locations of objects are used to predict their weights. Using location information, rather than the visual appearance of the objects, supports fast prediction, thereby avoiding processes that can be demanding on working memory.

Rapid Visuomotor Responses Reflect Value-Based Decisions.

Cognitive decision-making is known to be sensitive to the values of potential options, which are the probability and size of rewards associated with different choices. Here, we examine whether rapid motor responses to perturbations of visual feedback about movement, which mediate low-level and involuntary feedback control loops, reflect computations associated with high-level value-based decision-making. In three experiments involving human participants, we varied the value associated with different potential targets for reaching movements by controlling the distributions of rewards across the targets (Experiment 1), the probability with which each target could be specified (Experiment 2), or both (Experiment 3). We found that the size of rapid and involuntary feedback responses to movement perturbations was strongly influenced by the relative value between targets. A statistical model of relative value that includes a term for risk sensitivity provided the best fit to the visuomotor response data, illustrating that feedback control policies are biased to favor more frequent task success at the expense of the overall extrinsic reward accumulated through movement. Importantly however, the regulation of rapid feedback responses was associated with successful pursuit of high-value task outcomes. This implies that when we move, the brain specifies a set of feedback control gains that enable low-level motor areas not only to generate efficient and accurate movement, but also to rapidly and adaptively respond to evolving sensory information in a manner consistent with value-based decision-making.SIGNIFICANCE STATEMENT Current theories of sensorimotor control suggest that, rather than selecting and planning the details of movements in advance, the role of the brain is to set time-varying feedback gains that continuously transform sensory information into motor commands by feedback control. Here, we examine whether the fastest motor responses to perturbations of movement, which mediate low-level and involuntary feedback control loops (i.e., reflexes), reflect computations associated with high-level, value-based decision-making. We find that rapid feedback responses during reaching reflect the relative probabilities and rewards associated with target options. This suggests that low-order components of the sensorimotor control hierarchy, which generate rapid and automatic responses, can continuously evaluate evolving sensory evidence and initiate responses according to the prospect of reward.

Motor memories in manipulation tasks are linked to contact goals between objects.

Skillful manipulation requires forming memories of object dynamics, linking applied force to motion. Although it has been assumed that such memories are linked to objects, a recent study showed that people can form separate memories when these are linked to different controlled points on an object (Heald JB, Ingram JN, Flanagan JR, Wolpert DM. Nat Hum Behav 2: 300-311, 2018). In that study, participants controlled the handle of a robotic device to move a virtual bar with circles (control points) on the left and right sides. Participants were instructed to move either the left or right control point to a target on the left or right, respectively, such that the required movement was constant. When these control points were paired with opposing force fields, adaptation was observed. In this previous study, both the controlled point and the target changed between contexts. To assess which of these factors is critical for learning, here, we used a similar paradigm but with a bar that automatically rotated as it was moved. In the first experiment, the bar rotated, such that the left and right control points moved to a common target. In the second experiment, the bar rotated such that a single control point moved to a target located on either the left or right. In both experiments, participants were able to learn opposing force fields applied in the two contexts. We conclude that separate memories of dynamics can be formed for different "contact goals," involving a unique combination of the controlled point on an object and the target location this point "contacts."NEW & NOTEWORTHY Skilled manipulation requires forming memories of object dynamics, previously assumed to be associated with entire objects. However, we recently demonstrated that people can form multiple motor memories when explicitly instructed to move different locations on an object to different targets. Here, we show that separate motor memories can be learned for different contact goals, which involve a unique combination of a control point and target.

Separate motor memories are formed when controlling different implicitly specified locations on a tool.

Skillful manipulation requires forming and recalling memories of the dynamics of objects linking applied force to motion. It has been assumed that such memories are associated with entire objects. However, we often control different locations on an object, and these locations may be associated with different dynamics. We have previously demonstrated that multiple memories can be formed when participants are explicitly instructed to control different visual points marked on an object. A key question is whether this novel finding generalizes to more natural situations in which control points are implicitly defined by the task. To answer this question, we used objects with no explicit control points and tasks designed to encourage the use of distinct implicit control points. Participants moved a handle, attached to a robotic interface, to control the position of a rectangular object ("eraser") in the horizontal plane. Participants were required to move the eraser straight ahead to wipe away a column of dots ("dust"), located to either the left or right. We found that participants adapted to opposing dynamics when linked to the left and right dust locations, even though the movements required for these two contexts were the same. Control conditions showed this learning could not be accounted for by contextual cues or the fact that the task goal required moving in a straight line. These results suggest that people naturally control different locations on manipulated objects depending on the task context and that doing so affords the formation of separate motor memories. NEW & NOTEWORTHY Skilled manipulation requires forming motor memories of object dynamics, which have been assumed to be associated with entire objects. However, we recently demonstrated that people can form multiple memories when explicitly instructed to control different visual points on an object. In this article we show that this novel finding generalizes to more natural situations in which control points are implicitly defined by the task.

An error-tuned model for sensorimotor learning.

Current models of sensorimotor control posit that motor commands are generated by combining multiple modules which may consist of internal models, motor primitives or motor synergies. The mechanisms which select modules based on task requirements and modify their output during learning are therefore critical to our understanding of sensorimotor control. Here we develop a novel modular architecture for multi-dimensional tasks in which a set of fixed primitives are each able to compensate for errors in a single direction in the task space. The contribution of the primitives to the motor output is determined by both top-down contextual information and bottom-up error information. We implement this model for a task in which subjects learn to manipulate a dynamic object whose orientation can vary. In the model, visual information regarding the context (the orientation of the object) allows the appropriate primitives to be engaged. This top-down module selection is implemented by a Gaussian function tuned for the visual orientation of the object. Second, each module's contribution adapts across trials in proportion to its ability to decrease the current kinematic error. Specifically, adaptation is implemented by cosine tuning of primitives to the current direction of the error, which we show to be theoretically optimal for reducing error. This error-tuned model makes two novel predictions. First, interference should occur between alternating dynamics only when the kinematic errors associated with each oppose one another. In contrast, dynamics which lead to orthogonal errors should not interfere. Second, kinematic errors alone should be sufficient to engage the appropriate modules, even in the absence of contextual information normally provided by vision. We confirm both these predictions experimentally and show that the model can also account for data from previous experiments. Our results suggest that two interacting processes account for module selection during sensorimotor control and learning.

Enhanced crosslimb transfer of force-field learning for dynamics that are identical in extrinsic and joint-based coordinates for both limbs.

Humans are able to adapt their motor commands to make accurate movements in novel sensorimotor environments, such as when wielding tools that alter limb dynamics. However, it is unclear to what extent sensorimotor representations, obtained through experience with one limb, are available to the opposite, untrained limb and in which form they are available. Here, we compared crosslimb transfer of force-field compensation after participants adapted to a velocity-dependent curl field, oriented either in the sagittal or the transverse plane. Due to the mirror symmetry of the limbs, the force field had identical effects for both limbs in joint and extrinsic coordinates in the sagittal plane but conflicting joint-based effects in the transverse plane. The degree of force-field compensation exhibited by the opposite arm in probe trials immediately after initial learning was significantly greater after sagittal (26 ± 5%) than transverse plane adaptation (9 ± 4%; P < 0.001), irrespective of whether participants learned initially with the left or the right arm or via abrupt or gradual exposure to the force field. Thus transfer was impaired when the orientation of imposed dynamics conflicted in intrinsic coordinates for the two limbs. The data reveal that neural representations of novel dynamics are only partially available to the opposite limb, since transfer is incomplete even when force-field perturbation is spatially compatible for the two limbs, according to both intrinsic and extrinsic coordinates.

Ouvrai opens access to remote virtual reality studies of human behavioural neuroscience.

Modern virtual reality (VR) devices record six-degree-of-freedom kinematic data with high spatial and temporal resolution and display high-resolution stereoscopic three-dimensional graphics. These capabilities make VR a powerful tool for many types of behavioural research, including studies of sensorimotor, perceptual and cognitive functions. Here we introduce Ouvrai, an open-source solution that facilitates the design and execution of remote VR studies, capitalizing on the surge in VR headset ownership. This tool allows researchers to develop sophisticated experiments using cutting-edge web technologies such as WebXR to enable browser-based VR, without compromising on experimental design. Ouvrai's features include easy installation, intuitive JavaScript templates, a component library managing front- and backend processes and a streamlined workflow. It integrates with Firebase, Prolific and Amazon Mechanical Turk and provides data processing utilities for analysis. Unlike other tools, Ouvrai remains free, with researchers managing their web hosting and cloud database via personal Firebase accounts. Ouvrai is not limited to VR studies; researchers can also develop and run desktop or touchscreen studies using the same streamlined workflow. Through three distinct motor learning experiments, we confirm Ouvrai's efficiency and viability for conducting remote VR studies.

Exploration biases forelimb reaching strategies.

The brain can generate actions, such as reaching to a target, using different movement strategies. We investigate how such strategies are learned in a task where perched head-fixed mice learn to reach to an invisible target area from a set start position using a joystick. This can be achieved by learning to move in a specific direction or to a specific endpoint location. As mice learn to reach the target, they refine their variable joystick trajectories into controlled reaches, which depend on the sensorimotor cortex. We show that individual mice learned strategies biased to either direction- or endpoint-based movements. This endpoint/direction bias correlates with spatial directional variability with which the workspace was explored during training. Model-free reinforcement learning agents can generate both strategies with similar correlation between variability during training and learning bias. These results provide evidence that reinforcement of individual exploratory behavior during training biases the reaching strategies that mice learn.

Gone in 0.6 seconds: the encoding of motor memories depends on recent sensorimotor states.

Real-world tasks often require movements that depend on a previous action or on changes in the state of the world. Here we investigate whether motor memories encode the current action in a manner that depends on previous sensorimotor states. Human subjects performed trials in which they made movements in a randomly selected clockwise or counterclockwise velocity-dependent curl force field. Movements during this adaptation phase were preceded by a contextual phase that determined which of the two fields would be experienced on any given trial. As expected from previous research, when static visual cues were presented in the contextual phase, strong interference (resulting in an inability to learn either field) was observed. In contrast, when the contextual phase involved subjects making a movement that was continuous with the adaptation-phase movement, a substantial reduction in interference was seen. As the time between the contextual and adaptation movement increased, so did the interference, reaching a level similar to that seen for static visual cues for delays >600 ms. This contextual effect generalized to purely visual motion, active movement without vision, passive movement, and isometric force generation. Our results show that sensorimotor states that differ in their recent temporal history can engage distinct representations in motor memory, but this effect decays progressively over time and is abolished by ∼600 ms. This suggests that motor memories are encoded not simply as a mapping from current state to motor command but are encoded in terms of the recent history of sensorimotor states.

A single-rate context-dependent learning process underlies rapid adaptation to familiar object dynamics.

Motor learning has been extensively studied using dynamic (force-field) perturbations. These induce movement errors that result in adaptive changes to the motor commands. Several state-space models have been developed to explain how trial-by-trial errors drive the progressive adaptation observed in such studies. These models have been applied to adaptation involving novel dynamics, which typically occurs over tens to hundreds of trials, and which appears to be mediated by a dual-rate adaptation process. In contrast, when manipulating objects with familiar dynamics, subjects adapt rapidly within a few trials. Here, we apply state-space models to familiar dynamics, asking whether adaptation is mediated by a single-rate or dual-rate process. Previously, we reported a task in which subjects rotate an object with known dynamics. By presenting the object at different visual orientations, adaptation was shown to be context-specific, with limited generalization to novel orientations. Here we show that a multiple-context state-space model, with a generalization function tuned to visual object orientation, can reproduce the time-course of adaptation and de-adaptation as well as the observed context-dependent behavior. In contrast to the dual-rate process associated with novel dynamics, we show that a single-rate process mediates adaptation to familiar object dynamics. The model predicts that during exposure to the object across multiple orientations, there will be a degree of independence for adaptation and de-adaptation within each context, and that the states associated with all contexts will slowly de-adapt during exposure in one particular context. We confirm these predictions in two new experiments. Results of the current study thus highlight similarities and differences in the processes engaged during exposure to novel versus familiar dynamics. In both cases, adaptation is mediated by multiple context-specific representations. In the case of familiar object dynamics, however, the representations can be engaged based on visual context, and are updated by a single-rate process.

Separate representations of dynamics in rhythmic and discrete movements: evidence from motor learning.

Rhythmic and discrete arm movements occur ubiquitously in everyday life, and there is a debate as to whether these two classes of movements arise from the same or different underlying neural mechanisms. Here we examine interference in a motor-learning paradigm to test whether rhythmic and discrete movements employ at least partially separate neural representations. Subjects were required to make circular movements of their right hand while they were exposed to a velocity-dependent force field that perturbed the circularity of the movement path. The direction of the force-field perturbation reversed at the end of each block of 20 revolutions. When subjects made only rhythmic or only discrete circular movements, interference was observed when switching between the two opposing force fields. However, when subjects alternated between blocks of rhythmic and discrete movements, such that each was uniquely associated with one of the perturbation directions, interference was significantly reduced. Only in this case did subjects learn to corepresent the two opposing perturbations, suggesting that different neural resources were employed for the two movement types. Our results provide further evidence that rhythmic and discrete movements employ at least partially separate control mechanisms in the motor system.

Motor memories of object dynamics are categorically organized.

The ability to predict the dynamics of objects, linking applied force to motion, underlies our capacity to perform many of the tasks we carry out on a daily basis. Thus, a fundamental question is how the dynamics of the myriad objects we interact with are organized in memory. Using a custom-built three-dimensional robotic interface that allowed us to simulate objects of varying appearance and weight, we examined how participants learned the weights of sets of objects that they repeatedly lifted. We find strong support for the novel hypothesis that motor memories of object dynamics are organized categorically, in terms of families, based on covariation in their visual and mechanical properties. A striking prediction of this hypothesis, supported by our findings and not predicted by standard associative map models, is that outlier objects with weights that deviate from the family-predicted weight will never be learned despite causing repeated lifting errors.

Context-dependent partitioning of motor learning in bimanual movements.

Human subjects easily adapt to single dynamic or visuomotor perturbations. In contrast, when two opposing dynamic or visuomotor perturbations are presented sequentially, interference is often observed. We examined the effect of bimanual movement context on interference between opposing perturbations using pairs of contexts, in which the relative direction of movement between the two arms was different across the pair. When each perturbation direction was associated with a different bimanual context, such as movement of the arms in the same direction versus movement in the opposite direction, interference was dramatically reduced. This occurred over a short period of training and was seen for both dynamic and visuomotor perturbations, suggesting a partitioning of motor learning for the different bimanual contexts. Further support for this was found in a series of transfer experiments. Having learned a single dynamic or visuomotor perturbation in one bimanual context, subjects showed incomplete transfer of this learning when the context changed, even though the perturbation remained the same. In addition, we examined a bimanual context in which one arm was moved passively and show that the reduction in interference requires active movement. The sensory consequences of movement are thus insufficient to allow opposing perturbations to be co-represented. Our results suggest different bimanual movement contexts engage at least partially separate representations of dynamics and kinematics in the motor system.

Sensorimotor attenuation by central motor command signals in the absence of movement.

Voluntary actions typically produce suppression of afferent sensation from the moving body part. We used transcranial magnetic stimulation to delay the output of motor commands from the motor cortex during voluntary movement. We show attenuation of sensation during this delay, in the absence of movement. We conclude that sensory suppression mainly relies on central signals related to the preparation for movement and that these signals are upstream of primary motor cortex.

Age-related reduction in motor adaptation: brain structural correlates and the role of explicit memory.

The adaption of movement to changes in the environment varies across life span. Recent evidence has linked motor adaptation and its reduction with age to differences in "explicit" learning processes. We examine differences in brain structure and cognition underlying motor adaptation in a population-based cohort (n = 322, aged 18-89 years) using a visuomotor learning task and structural magnetic resonance imaging. Reduced motor adaptation with age was associated with reduced volume in striatum, prefrontal, and sensorimotor cortical regions, but not cerebellum. Medial temporal lobe volume, including the hippocampus, became a stronger determinant of motor adaptation with age. Consistent with the role of the medial temporal lobes, declarative long-term memory showed a similar interaction, whereby memory was more positively correlated with motor adaptation with increasing age. By contrast, visual short-term memory was related to motor adaptation, independently of age. These results support the hypothesis that cerebellar learning is largely unaffected in old age, and the reduction in motor adaptation with age is driven by a decline in explicit memory systems.

Composition and decomposition in bimanual dynamic learning.

Our ability to skillfully manipulate an object often involves the motor system learning to compensate for the dynamics of the object. When the two arms learn to manipulate a single object they can act cooperatively, whereas when they manipulate separate objects they control each object independently. We examined how learning transfers between these two bimanual contexts by applying force fields to the arms. In a coupled context, a single dynamic is shared between the arms, and in an uncoupled context separate dynamics are experienced independently by each arm. In a composition experiment, we found that when subjects had learned uncoupled force fields they were able to transfer to a coupled field that was the sum of the two fields. However, the contribution of each arm repartitioned over time so that, when they returned to the uncoupled fields, the error initially increased but rapidly reverted to the previous level. In a decomposition experiment, after subjects learned a coupled field, their error increased when exposed to uncoupled fields that were orthogonal components of the coupled field. However, when the coupled field was reintroduced, subjects rapidly readapted. These results suggest that the representations of dynamics for uncoupled and coupled contexts are partially independent. We found additional support for this hypothesis by showing significant learning of opposing curl fields when the context, coupled versus uncoupled, was alternated with the curl field direction. These results suggest that the motor system is able to use partially separate representations for dynamics of the two arms acting on a single object and two arms acting on separate objects.

The visual geometry of a tool modulates generalization during adaptation.

Knowledge about a tool's dynamics can be acquired from the visual configuration of the tool and through physical interaction. Here, we examine how visual information affects the generalization of dynamic learning during tool use. Subjects rotated a virtual hammer-like object while we varied the object dynamics separately for two rotational directions. This allowed us to quantify the coupling of adaptation between the directions, that is, how adaptation transferred from one direction to the other. Two groups experienced the same dynamics of the object. For one group, the object's visual configuration was displayed, while for the other, the visual display was uninformative as to the dynamics. We fit a range of context-dependent state-space models to the data, comparing different forms of coupling. We found that when the object's visual configuration was explicitly provided, there was substantial coupling, such that 31% of learning in one direction transferred to the other. In contrast, when the visual configuration was ambiguous, despite experiencing the same dynamics, the coupling was reduced to 12%. Our results suggest that generalization of dynamic learning of a tool relies, not only on its dynamic behaviour, but also on the visual configuration with which the dynamics is associated.

Unimodal statistical learning produces multimodal object-like representations.

The concept of objects is fundamental to cognition and is defined by a consistent set of sensory properties and physical affordances. Although it is unknown how the abstract concept of an object emerges, most accounts assume that visual or haptic boundaries are crucial in this process. Here, we tested an alternative hypothesis that boundaries are not essential but simply reflect a more fundamental principle: consistent visual or haptic statistical properties. Using a novel visuo-haptic statistical learning paradigm, we familiarised participants with objects defined solely by across-scene statistics provided either visually or through physical interactions. We then tested them on both a visual familiarity and a haptic pulling task, thus measuring both within-modality learning and across-modality generalisation. Participants showed strong within-modality learning and 'zero-shot' across-modality generalisation which were highly correlated. Our results demonstrate that humans can segment scenes into objects, without any explicit boundary cues, using purely statistical information.

The statistics of natural hand movements.

Humans constantly use their hands to interact with the environment and they engage spontaneously in a wide variety of manual activities during everyday life. In contrast, laboratory-based studies of hand function have used a limited range of predefined tasks. The natural movements made by the hand during everyday life have thus received little attention. Here, we developed a portable recording device that can be worn by subjects to track movements of their right hand as they go about their daily routine outside of a laboratory setting. We analyse the kinematic data using various statistical methods. Principal component analysis of the joint angular velocities showed that the first two components were highly conserved across subjects, explained 60% of the variance and were qualitatively similar to those reported in previous studies of reach-to-grasp movements. To examine the independence of the digits, we developed a measure based on the degree to which the movements of each digit could be linearly predicted from the movements of the other four digits. Our independence measure was highly correlated with results from previous studies of the hand, including the estimated size of the digit representations in primary motor cortex and other laboratory measures of digit individuation. Specifically, the thumb was found to be the most independent of the digits and the index finger was the most independent of the fingers. These results support and extend laboratory-based studies of the human hand.

Adaptive coupling influences generalization of sensorimotor learning.

Sensorimotor learning typically shows generalization from one context to another. Models of sensorimotor learning characterize this with a fixed generalization function that couples learning between contexts. Here we examine whether such coupling is indeed fixed or changes with experience. We examine the interaction between motor memories for novel dynamics during reciprocating, back and forth reaching movements. Subjects first experienced a force field for one movement direction and we used channel trials to assess generalization on the reciprocal movements. This showed minimal coupling such that errors experienced for one movement direction did not lead to adaptation for the other. However, after subjects had experienced a force field for both movement directions concurrently, a coupling developed between the corresponding motor memories. That is, on re-exposure for one direction there was a significant adaptation for movements in the other direction. The coupling was specific to the errors experienced, with minimal coupling when the errors had the opposite sign to those experienced during adaptation. We developed a state-space model in which the states for the two movement directions are represented by separate, yet potentially coupled learning processes. The coupling in the model controlled the extent to which each learning process was updated by the errors experienced on the other movement direction. We show that the coupling relies on a memory trace of the consecutive errors experienced for both movement directions. Our results suggest that the generalization of motor learning is an adaptive process, reflecting the relation between errors experienced across different movements.