Repeated context-specific actions disrupt feedforward adjustments in motor commands in younger and older adults.

The flexibility of the motor system to adjust a planned action before or during the execution of the movement in response to sensory information is critical for preventing errors in motor control. As individuals age, this function declines, leading to an increased incidence of motor errors. Although sensory processing and cognitive decline are known contributors to this impairment, here, we test the hypothesis that repetition of context-specific planned actions interferes with the adjustment of feedforward motor commands. Younger and older participants were instructed to grasp and lift a T-shaped object with a concealed, off-sided center of mass and minimize its roll through anticipatory force control, relying predominantly on predictive model-driven planning (i.e., sensorimotor memories) developed through repeated lifts. We selectively manipulate the number of trial repeats with the center of mass on one side before switching it to the other side of the T-shaped object. The results showed that increasing the number of repetitions improved performance in manipulating an object with a given center of mass but led to increased errors when the object's center of mass was switched. This deleterious effect of repetition on feedforward motor adjustment was observed in younger and older adults. Critically, we show these effects on an internal model-driven motor planning task that relies predominantly on sensorimotor memory, with no differences in sensory inputs from the repetition manipulation. The findings indicate that feedforward motor adjustments are hampered by repetitive stereotyped planning and execution of motor behavior.NEW & NOTEWORTHY Adjusting planned actions in response to sensory stimuli degrades with age contributing to increased incidence of errors ranging from clumsy spills to catastrophic falls. Multiple factors likely contribute to age-related motor inflexibility, including sensory- and cognition-supporting system declines. Here, we present compelling evidence for repetition to disrupt feedforward adjusting of motor commands in younger and older adults, which suggests increases in stereotypy as a deleterious potentiator of motor control errors.

Reorganization of sensorimotor representations of the intact limb after upper but not lower limb traumatic amputation.

It is becoming increasingly clear that limb loss induces wider spread reorganization of representations of the body that are nonadjacent to the affected cortical territory. Data from upper extremity amputees reveal intrusion of the representation of the ipsilateral intact limb into the former hand territory. Here we test for the first time whether this reorganization of the intact limb into the deprived cortex is specific to the neurological organization of the upper limbs or reflects large scale adaptation that is triggered by any unilateral amputation. BOLD activity was measured as human subjects with upper limb and lower limb traumatic amputation and their controls moved the toes on each foot, open and closed each hand and pursed their lips. Subjects with amputation were asked to imagine moving the missing limb while remaining still. Bayesian pattern component modeling of fMRI data showed that intact ipsilateral movements and contralateral movements of the hand and foot were distinctly represented in the deprived sensorimotor cortex years after upper limb amputation. In contrast, there was evidence reminiscent of contralateral specificity for hand and foot movements following lower limb amputation, like that seen in controls. We propose the cortical reorganization of the intact limb to be a function of use-dependent plasticity that is more specific to the consequence of upper limb loss of forcing an asymmetric reliance on the intact hand and arm. The contribution of this reorganization to phantom pain or a heightened risk of overuse and resultant maladaptive plasticity needs investigating before targeting such reorganization in intervention.

Visual information following object grasp supports digit position variability and swift anticipatory force control.

Anticipatory force control underlying dexterous manipulation has historically been understood to rely on visual object properties and on sensorimotor memories associated with previous experiences with similar objects. However, it is becoming increasingly recognized that anticipatory force control also relies on how an object is grasped. Experiments that allow unconstrained grasp contact points when preventing tilting an object with an off-centered mass show trial-to-trial variations in digit position and subsequent scaling of lift forces, all before feedback of object properties becomes available. Here, we manipulated the availability of visual information before reach onset and after grasp contact (with no vision during the reach) to determine the contribution and timing of visual information processing to the scaling of fingertip forces during dexterous manipulation at flexible contact points. Results showed that anticipatory force control was similarly successful, quantified as an appropriate compensatory torque at lift onset that counters the external torque of an object with a left and right center of mass, irrespective of the timing and availability of visual information. However, the way in which anticipatory force control was achieved varied depending on the availability of visual information. Visual information following grasp contact was associated with greater use of an asymmetric thumb and index finger grasp configuration to generate a compensatory torque and digit position variability, together with faster fingertip force scaling and sensorimotor learning. This result supports the hypothesis that visual information at a critical and functionally relevant time point following grasp contact supports variable and swift digit-based force control for dexterous object manipulation.NEW & NOTEWORTHY Humans excel in dexterous object manipulation by precisely coordinating grasp points and fingertip forces, highlighted in scenarios requiring countering object torques in advance, e.g., lifting a teacup without spilling will demand a unique digit force pattern based on the grip configuration at lift onset. Here, we show that visual information following grasp contact, a critical and functionally relevant time point, supports digit position variability and swift anticipatory force control to achieve a dexterous motor goal.

Motor adaptation via distributional learning.

Objective. Both artificial and biological controllers experience errors during learning that are probabilistically distributed. We develop a framework for modeling distributions of errors and relating deviations in these distributions to neural activity.Approach. The biological system we consider is a task where human subjects are required to learn to minimize the roll of an inverted T-shaped object with an unbalanced weight (i.e. one side of the object is heavier than the other side) during lift. We also collect BOLD activity during this process. For our experimental setup, we define the state of the system to be the maximum magnitude roll of the object after lift onset and give subjects the goal of achieving the zero state.Main Results. We derive a model for this problem from a variant of Temporal Difference Learning. We then combine this model with Distributional Reinforcement Learning (DRL), a framework that involves defining a value distribution by treating the reward as stochastic. This model transforms the goal of the controller from achieving a target state, to achieving a distribution over distances from the target state. We call it a Distributional Temporal Difference Model (DTDM). The DTDM allows us to model errors in unsuccessfully minimizing object roll using deviations in the value distribution when the center of mass of the unbalanced object is changed. We compute deviations in global neural activity and show that they vary continuously with deviations in the value distribution. Different aspects might contribute to this global shift or signal difference, including a difference in grasp and lift force at lift onset, as well as sensory feedback of error/roll after lift onset. We predict that there exists a coordinated, global response to errors that incorporates all of this information, which is encoding the DTDM objective and used on subsequent trials enabling success. We validate the utility of the DTDM as a model for biological adaptation by using it to engineer a robotic controller to solve a similar problem.Significance. We develop a novel theoretical framework and show that it can be used to model a non-trivial motor learning task. Because this theoretical framework is consistent with state-of-the-art reinforcement learning, we can also use it to program a robot to perform a similar task. These results suggest a way to model the multiple subsystems composing global neural activity in a way that transfers well to engineering artificial intelligence.

Neural substrates of anticipatory motor adaptation for object lifting.

Anticipatory force control is a fundamental means by which humans stave off slipping, spilling, and tilting disasters while manipulating objects. This control must often be adapted due to changes in an object's dynamics (e.g. a lighter than expected mug of coffee) or its relation with involved effectors or digits (e.g. lift a mug with three vs. five digits). The neural processes guiding such anticipatory and adaptive control is understudied but presumably operates along multiple time scales, analogous to what has been identified with adaptation in other motor tasks, such as perturbations during reaching. Learning of anticipatory forces must be ultrafast to minimize tilting a visually symmetric object towards its concealed asymmetric center of mass (CoM), but slower when the CoM is explicitly and systematically switched from side to side. Studying the neural substrates of this latter slower learning process with rapid multiband brain imaging, in-scanner kinematics and Bayesian pattern component modelling, we show that CoM-specific pattern distances increase with repeated CoM switching exposures and improved learning. The cerebellum showed the most prominent effects, fitting with the idea that it forms a stored internal model that is used to build and update anticipatory control. CoM-specific pattern distances were present 24 h later, in line with the presence of consolidation effects.

Representational Neural Mapping of Dexterous Grasping Before Lifting in Humans.

The ability of humans to reach and grasp objects in their environment has been the mainstay paradigm for characterizing the neural circuitry driving object-centric actions. Although much is known about hand shaping, a persistent question is how the brain orchestrates and integrates the grasp with lift forces of the fingers in a coordinated manner. The objective of the current study was to investigate how the brain represents grasp configuration and lift force during a dexterous object-centric action in a large sample of male and female human subjects. BOLD activity was measured as subjects used a precision-grasp to lift an object with a center of mass (CoM) on the left or right with the goal of minimizing tilting the object. The extent to which grasp configuration and lift force varied between left and right CoM conditions was manipulated by grasping the object collinearly (requiring a non-collinear force distribution) or non-collinearly (requiring more symmetrical forces). Bayesian variational representational similarity analyses on fMRI data assessed the evidence that a set of cortical and cerebellar regions were sensitive to grasp configuration or lift force differences between CoM conditions at differing time points during a grasp to lift action. In doing so, we reveal strong evidence that grasping and lift force are not represented by spatially separate functionally specialized regions, but by the same regions at differing time points. The coordinated grasp to lift effort is shown to be under dorsolateral (PMv and AIP) more than dorsomedial control, and under SPL7, somatosensory PSC, ventral LOC and cerebellar control.SIGNIFICANCE STATEMENT Clumsy disasters such as spilling, dropping, and crushing during our daily interactions with objects are a rarity rather than the norm. These disasters are avoided in part as a result of our orchestrated anticipatory efforts to integrate and coordinate grasping and lifting of object interactions, all before the lift of an object even commences. How the brain orchestrates this integration process has been largely neglected by historical approaches independently and solely focusing on reaching and grasping and the neural principles that guide them. Here, we test the extent to which grasping and lifting are represented in a spatially or temporally distinct manner and identified strong evidence for the consecutive emergence of sensitivity to grasping, then lifting within the same region.

Overt and Covert Object Features Mediate Timing of Patterned Brain Activity during Motor Planning.

Humans are seamless in their ability to efficiently and reliably generate fingertip forces to gracefully interact with objects. Such interactions rarely end in awkward outcomes like spilling, crushing, or tilting given advanced motor planning. Here we combine multiband imaging with deconvolution- and Bayesian pattern component modeling of functional magnetic resonance imaging data and in-scanner kinematics, revealing compelling evidence that the human brain differentially represents preparatory information for skillful object interactions depending on the saliency of visual cues. Earlier patterned activity was particularly evident in ventral visual processing stream-, but also selectively in dorsal visual processing stream and cerebellum in conditions of heightened uncertainty when an object's superficial shape was incompatible rather than compatible with a key underlying object feature.

Neural Representations of Sensorimotor Memory- and Digit Position-Based Load Force Adjustments Before the Onset of Dexterous Object Manipulation.

Anticipatory load forces for dexterous object manipulation in humans are modulated based on visual object property cues, sensorimotor memories of previous experiences with the object, and, when digit positioning varies from trial to trial, the integrating of this sensed variability with force modulation. Studies of the neural representations encoding these anticipatory mechanisms have not considered these mechanisms separately from each other or from feedback mechanisms emerging after lift onset. Here, representational similarity analyses of fMRI data were used to identify neural representations of sensorimotor memories and the sensing and integration of digit position. Cortical activity and movement kinematics were measured as 20 human subjects (11 women) minimized tilt of a symmetrically shaped object with a concealed asymmetric center of mass (CoM, left and right sided). This task required generating compensatory torques in opposite directions, which, without helpful visual CoM cues, relied primarily on sensorimotor memories of the same object and CoM. Digit position was constrained or unconstrained, the latter of which required modulating forces beyond what can be recalled from sensorimotor memories to compensate for digit position variability. Ventral premotor (PMv), somatosensory, and cerebellar lobule regions (CrusII, VIIIa) were sensitive to anticipatory behaviors that reflect sensorimotor memory content, as shown by larger voxel pattern differences for unmatched than matched CoM conditions. Cerebellar lobule I-IV, Broca area 44, and PMv showed greater voxel pattern differences for unconstrained than constrained grasping, which suggests their sensitivity to monitor the online coincidence of planned and actual digit positions and correct for a mismatch by force modulation.SIGNIFICANCE STATEMENT To pick up a water glass without slipping, tipping, or spilling requires anticipatory planning of fingertip load forces before the lift commences. This anticipation relies on object visual properties (e.g., mass/mass distribution), sensorimotor memories built from previous experiences (especially when object properties cannot be inferred visually), and online sensing of where the digits are positioned. There is limited understanding of how the brain represents each of these anticipatory mechanisms. We used fMRI measures of regional brain patterns and digit position kinematics before lift onset of an object with nonsalient visual cues specifically to isolate sensorimotor memories and integration of sensed digit position with force modulation. In doing so, we localized neural representations encoding these anticipatory mechanisms for dexterous object manipulation.

The Relationship Between Hand Function and Overlapping Motor Representations of the Hands in the Contralesional Hemisphere in Unilateral Spastic Cerebral Palsy.

BACKGROUND: In many children with unilateral spastic cerebral palsy (USCP), the corticospinal tract to the affected hand atypically originates in the hemisphere ipsilateral to the affected hand. Such ipsilateral connectivity is on average a predictor of poor hand function. However, there is high variability in hand function in these children, which might be explained by the complexity of motor representations of both hands in the contralesional hemisphere. OBJECTIVE: To measure the link between hand function and the size and excitability of motor representations of both hands, and their overlap, in the contralesional hemisphere of children with USCP. METHODS: We used single-pulse transcranial magnetic stimulation to measure the size and excitability of motor representations of both hands, and their overlap, in the contralesional hemisphere of 50 children with USCP. We correlated these measures with manual dexterity of the affected hand, bimanual performance, and mirror movement strength. RESULTS: The main and novel findings were (1) the large overlap in contralesional motor representations of the 2 hands and (2) the moderate positive associations of the size and excitability of such shared-site representations with hand function. Such functional associations were not present for overall size and excitability of representations of the affected hand. CONCLUSIONS: Greater relative overlap of the affected hand representation with the less-affected hand representation within the contralesional hemisphere was associated with better hand function. This association suggests that overlapping representations might be adaptively "yoked," such that cortical control of the child's less-affected hand supports that of the affected hand.

Digit Position and Forces Covary during Anticipatory Control of Whole-Hand Manipulation.

Theoretical perspectives on anticipatory planning of object manipulation have traditionally been informed by studies that have investigated kinematics (hand shaping and digit position) and kinetics (forces) in isolation. This poses limitations on our understanding of the integration of such domains, which have recently been shown to be strongly interdependent. Specifically, recent studies revealed strong covariation of digit position and load force during the loading phase of two-digit grasping. Here, we determined whether such digit force-position covariation is a general feature of grasping. We investigated the coordination of digit position and forces during five-digit whole-hand manipulation of an object with a variable mass distribution. Subjects were instructed to prevent object roll during the lift. As found in precision grasping, there was strong trial-to-trial covariation of digit position and force. This suggests that the natural variation of digit position that is compensated for by trial-to-trial variation in digit forces is a fundamental feature of grasp control, and not only specific to precision grasp. However, a main difference with precision grasping was that modulation of digit position to the object's mass distribution was driven predominantly by the thumb, with little to no modulation of finger position. Modulation of thumb position rather than fingers is likely due to its greater range of motion and therefore adaptability to object properties. Our results underscore the flexibility of the central nervous system in implementing a range of solutions along the digit force-to-position continuum for dexterous manipulation.

Visual Cues of Object Properties Differentially Affect Anticipatory Planning of Digit Forces and Placement.

Studies on anticipatory planning of object manipulation showed initial task failure (i.e., object roll) when visual object shape cues are incongruent with other visual cues, such as weight distribution/density (e.g., symmetrically shaped object with an asymmetrical density). This suggests that shape cues override density cues. However, these studies typically only measured forces, with digit placement constrained. Recent evidence suggests that when digit placement is unconstrained, subjects modulate digit forces and placement. Thus, unconstrained digit placement might be modulated on initial trials (since it is an explicit process), but not forces (since it is an implicit process). We tested whether shape and density cues would differentially influence anticipatory planning of digit placement and forces during initial trials of a two-digit object manipulation task. Furthermore, we tested whether shape cues would override density cues when cues are incongruent. Subjects grasped and lifted an object with the aim of preventing roll. In Experiment 1, the object was symmetrically shaped, but with asymmetrical density (incongruent cues). In Experiment 2, the object was asymmetrical in shape and density (congruent cues). In Experiment 3, the object was asymmetrically shaped, but with symmetrical density (incongruent cues). Results showed differential modulation of digit placement and forces (modulation of load force but not placement), but only when shape and density cues were congruent. When shape and density cues were incongruent, we found collinear digit placement and symmetrical force sharing. This suggests that congruent and incongruent shape and density cues differentially influence anticipatory planning of digit forces and placement. Furthermore, shape cues do not always override density cues. A continuum of visual cues, such as those alluding to shape and density, need to be integrated.

Elucidating the neural circuitry underlying planning of internally-guided voluntary action.

In an attempt to elucidate the neural circuitry of planning of internally guided voluntary action, Ariani et al. (2015) used a delayed-movement design and multivariate pattern analysis of functional MRI data and found areas decoding internally elicited action plans, stimulus-elicited action plans, and both types of plans. In interpreting their results in the context of a heuristic decision model of voluntary action, encompassing "what" action to perform, "when" to perform it, and "whether" to perform it at all, we highlight at least some neural dissociation of these components. More to that, we note that the exact neural circuitry of each component might vary depending on the performed action type, and finally, we underscore the importance of understanding the temporal specifics of such circuitries to further elucidate how they are involved and interact during voluntary action planning.

The neural bases of different levels of action understanding.

Many have recently questioned whether all levels of actions understanding, from lower kinematic levels to the higher goal or intention levels of action understanding, are processed in the action observation network (a network of neurons that are active during action execution and observation). A recent study by Wurm and Lingnau (J Neurosci 35: 7727-7735, 2015) gave evidence to the contrary, by showing that higher levels of action understanding are processed in the lateral occipitotemporal cortex. An important next step is to differentiate between the role of the lateral occipitotemporal cortex in processing the visual form of an observed action and the goal of an observed action.

Generalization of Dexterous Manipulation Is Sensitive to the Frame of Reference in Which It Is Learned.

Studies have shown that internal representations of manipulations of objects with asymmetric mass distributions that are generated within a specific orientation are not generalizable to novel orientations, i.e., subjects fail to prevent object roll on their first grasp-lift attempt of the object following 180° object rotation. This suggests that representations of these manipulations are specific to the reference frame in which they are formed. However, it is unknown whether that reference frame is specific to the hand, the body, or both, because rotating the object 180° modifies the relation between object and body as well as object and hand. An alternative, untested explanation for the above failure to generalize learned manipulations is that any rotation will disrupt grasp performance, regardless if the reference frame in which the manipulation was learned is maintained or modified. We examined the effect of rotations that (1) maintain and (2) modify relations between object and body, and object and hand, on the generalizability of learned two-digit manipulation of an object with an asymmetric mass distribution. Following rotations that maintained the relation between object and body and object and hand (e.g., rotating the object and subject 180°), subjects continued to use appropriate digit placement and load force distributions, thus generating sufficient compensatory moments to minimize object roll. In contrast, following rotations that modified the relation between (1) object and hand (e.g. rotating the hand around to the opposite object side), (2) object and body (e.g. rotating subject and hand 180°), or (3) both (e.g. rotating the subject 180°), subjects used the same, yet inappropriate digit placement and load force distribution, as those used prior to the rotation. Consequently, the compensatory moments were insufficient to prevent large object rolls. These findings suggest that representations of learned manipulation of objects with asymmetric mass distributions are specific to the body- and hand-reference frames in which they were learned.

Voluntary control of facial musculature in Parkinson's disease.

Aside from being measured in the context of producing facial expressions of emotion, the ability to voluntarily control a range of facial muscles in Parkinson's disease (PD) has not been systematically measured. We used in three enrollment phases an adaptation of the Upper and Lower Face Apraxia test, a measure of the ability to make voluntary movements of the upper and lower face in PD patients and healthy controls. Errors were scored due to (1) pauses prior to movement initiation, (2) loss of individuation, (3) impoverished movement, (4) no movement at all, or (5) content errors (likened to ideational apraxia errors). The results show impaired voluntary control of facial musculature in most but not all with PD (with large effect sizes) which correlated positively and highly with disease severity. Errors by PD patients were predominantly due to impoverished movement and individuation loss whereas those made by controls were predominantly due to individuation loss. Patients committed more errors than controls due to impoverishment and no movement, with negligible differences between groups in other errors. In summary, similarly to spontaneous and voluntary emotional expressions, voluntary non-emotional facial movements are impoverished in PD; impoverishment of all movement types will likely contribute to the mask-like facial appearance that is seen with disease progression. These findings also illustrate the utility of an adapted Face Apraxia test as a practical and sensitive measure of voluntary facial musculature control in PD. The test can be used to supplement clinical observations and as a research tool.

Discriminating facial expressions of emotion and its link with perceiving visual form in Parkinson's disease.

We investigated the link between the ability to perceive facial expressions of emotion and the ability to perceive visual form in Parkinson's disease (PD). We assessed in individuals with PD and healthy controls the ability to discriminate graded intensities of facial expressions of anger from neutral expressions and the ability to discriminate radial frequency (RF) patterns with modulations in amplitude from a perfect circle. Those with PD were, as a group, impaired relative to controls in discriminating graded intensities of angry from neutral expressions and discriminating modulated amplitudes of RF patterns from perfect circles; these two abilities correlated positively and moderately to highly, even after removing the variance that was shared with disease progression and general cognitive functioning. The results indicate that the impaired ability to perceive visual form is likely to contribute to the impaired ability to perceive facial expressions of emotion in PD, and that both are related to the progression of the disease.

Discrimination and recognition of facial expressions of emotion and their links with voluntary control of facial musculature in Parkinson's disease.

OBJECTIVE: To explore perception of facial expressions of emotion and its link with voluntary facial musculature control in Parkinson's disease (PD). METHOD: We investigated in 2 sets of experiments in PD patients and healthy controls the perceptual ability to discriminate (a) graded intensities of emotional from neutral expressions, (b) graded intensities of the same emotional expressions, (c) full-blown discrepant emotional expressions from 2 similar expressions and the more complex recognition ability to label full-blown emotional expressions. We tested an embodied simulationist account of emotion perception in PD, which predicts a link between the ability to perceive emotional expressions and facial musculature control. We also explored the contribution of the ability to extract facial information (besides emotion) to emotion perception in PD. RESULTS: Those with PD were, as a group, impaired relative to controls (with large effect sizes) in all measures of discrimination and recognition of emotional expressions, although some patients performed as well as the best performing controls. In support of embodied simulation, discrimination and recognition of emotional expressions correlated positively with voluntary control of facial musculature (after partialing out disease severity and age). Patients were also impaired at extracting information other than emotion from faces, specifically discriminating and recognizing identity from faces (with large effect sizes); identity discrimination correlated positively with emotion discrimination and recognition but not with voluntary facial musculature control (after partialing out disease severity and age). CONCLUSIONS: The results indicate that impaired sensory and sensorimotor processes, which are a function of disease severity, affect emotion perception in PD.

Psychophysical measures of sensitivity to facial expression of emotion.

We report the development of two simple, objective, psychophysical measures of the ability to discriminate facial expressions of emotion that vary in intensity from a neutral facial expression and to discriminate between varying intensities of emotional facial expression. The stimuli were created by morphing photographs of models expressing four basic emotions, anger, disgust, happiness, and sadness with neutral expressions. Psychometric functions were obtained for 15 healthy young adults using the Method of Constant Stimuli with a two-interval forced-choice procedure. Individual data points were fitted by Quick functions for each task and each emotion, allowing estimates of absolute thresholds and slopes. The tasks give objective and sensitive measures of the basic perceptual abilities required for perceiving and interpreting emotional facial expressions.

Short-interval intracortical inhibition and manual dexterity in healthy aging.

Short-interval intracortical inhibition (SICI) acting on the first dorsal interosseus was measured using paired-pulse transcranial magnetic stimulation (interstimulus interval=2ms) in samples of young and healthy older subjects and correlated with manual dexterity measured with the Purdue Pegboard test and two isometric force-matching tasks. There was an age-related decrease in SICI and an age-related decline in all dexterity measures. The level of SICI was not correlated with any of the dexterity measures, but the appearance of atypical facilitation (rather than inhibition) in some subjects was associated with impaired pegboard performance but not force-matching performance. We conclude that SICI at rest is reduced with healthy aging but this loss of SICI does not directly contribute to the loss of dexterity; a shift in the balance of facilitatory and inhibitory processes in motor cortex to facilitation might interfere with sequenced hand movements.