Single-Trial Dynamics of Competing Reach Plans in the Human Motor Periphery.

Contemporary motor control theories propose competition between multiple motor plans before the winning command is executed. While most competitions are completed before movement onset, movements are often initiated before the competition has been resolved. An example of this is saccadic averaging, wherein the eyes land at an intermediate location between two visual targets. Behavioral and neurophysiological signatures of competing motor commands have also been reported for reaching movements, but debate remains about whether such signatures attest to an unresolved competition, arise from averaging across many trials, or reflect a strategy to optimize behavior given task constraints. Here, we recorded EMG activity from an upper limb muscle (m. pectoralis) while 12 (8 female) participants performed an immediate response reach task, freely choosing between one of two identical and suddenly presented visual targets. On each trial, muscle recruitment showed two distinct phases of directionally tuned activity. In the first wave, time-locked ∼100 ms of target presentation, muscle activity was clearly influenced by the nonchosen target, reflecting a competition between reach commands that was biased in favor of the ultimately chosen target. This resulted in an initial movement intermediate between the two targets. In contrast, the second wave, time-locked to voluntary reach onset, was not biased toward the nonchosen target, showing that the competition between targets was resolved. Instead, this wave of activity compensated for the averaging induced by the first wave. Thus, single-trial analysis reveals an evolution in how the nonchosen target differentially influences the first and second wave of muscle activity.SIGNIFICANCE STATEMENT Contemporary theories of motor control suggest that multiple motor plans compete for selection before the winning command is executed. Evidence for this is found in intermediate reach movements toward two potential target locations, but recent findings have challenged this notion by arguing that intermediate reaching movements reflect an optimal response strategy. By examining upper limb muscle recruitment during a free-choice reach task, we show early recruitment of a suboptimal averaged motor command to the two targets that subsequently transitions to a single motor command that compensates for the initially averaged motor command. Recording limb muscle activity permits single-trial resolution of the dynamic influence of the nonchosen target through time.

Abrupt, but not gradual, motor adaptation biases saccadic target selection.

Motor costs influence movement selection. These costs could change when movements are adapted in response to errors. When the motor system attributes the encountered errors to an external cause, appropriate movement selection requires an update of the movement goal, which prompts the selection of a different control policy. However, when errors are attributed to an internal cause, the initially selected control policy could remain unchanged, but the internal forward model of the body needs to be updated, resulting in an online correction of the movement. We hypothesized that external attribution of errors leads to the selection of a different control policy, and thus to a change in the expected cost of movements. This should also affect subsequent motor decisions. Conversely, internal attribution of errors may (initially) only evoke online corrections, and thus is expected to leave the motor decision process unchanged. We tested this hypothesis using a saccadic adaptation paradigm, designed to change the relative motor cost of two targets. Motor decisions were measured using a target selection task between the two saccadic targets before and after adaptation. Adaptation was induced by either abrupt or gradual perturbation schedules, which are thought to induce more external or internal attribution of errors, respectively. By taking individual variability into account, our results show that saccadic decisions shift toward the least costly target after adaptation, but only when the perturbation is abruptly, and not gradually, introduced. We suggest that credit assignment of errors not only influences motor adaptation but also subsequent motor decisions.NEW & NOTEWORTHY Decisions between potential motor actions are influenced by their costs, but costs change when movements are adapted. Using a saccadic target selection task, we show that target preference shifts after abrupt, but not after gradual adaptation. We suggest that this difference emerges because abrupt adaptation results in target remapping, and thus directly influences cost calculations, whereas gradual adaptation is mainly driven by corrections to a forward model that is not involved in cost calculations.

Plan- versus motion-referenced generalization of fast and slow processes in reach adaptation.

Generalization in motor learning refers to the transfer of a learned compensation to other relevant contexts. The generalization function is typically assumed to be of Gaussian shape, centered on the planned motion, although more recent studies associate generalization with the actual motion. Because motor learning is thought to involve multiple adaptive processes with different time constants, we hypothesized that these processes have different time-dependent contributions to the generalization. Guided by a model-based approach, the objective of the present study was to experimentally examine these contributions. We first reformulated a validated two-state adaptation model as a combination of weighted motor primitives, each specified as a Gaussian-shaped tuning function. Adaptation in this model is achieved by updating individual weights of the primitives of the fast and slow adaptive process separately. Depending on whether updating occurred in a plan-referenced or a motion-referenced manner, the model predicted distinct contributions to the overall generalization by the slow and fast process. We tested 23 participants in a reach adaptation task, using a spontaneous recovery paradigm consisting of five successive blocks of a long adaptation phase to a viscous force field, a short adaptation phase with the opposite force, and an error-clamp phase. Generalization was assessed in 11 movement directions relative to the trained target direction. Results of our participant population fell within a continuum of evidence for plan-referenced to evidence for motion-referenced updating. This mixture may reflect the differential weighting of explicit and implicit compensation strategies among participants.NEW & NOTEWORTHY Error-based reach adaptation can be modeled by fast and slow adaptive processes. Using a spontaneous recovery paradigm and model-based analyses, we tested how these processes generalize during force-field reach adaptation. Depending on whether the fast and slow adaptive processes operate by crediting the planned or actual motion, the model predicts distinct contributions of them to the overall generalization function. We show that human participants fall within a continuum of evidence for plan-referenced to motion-referenced updating.

Muscular reflex gains reflect changes of mind in reaching.

Decisions for action are accompanied by a continual processing of sensory information, sometimes resulting in a revision of the initial choice, called a change of mind (CoM). Although the motor system is tuned during the formation of a reach decision, it is unclear whether its preparatory state differs between CoM and non-CoM decisions. To test this, participants (n = 14) viewed a random-dot motion (RDM) stimulus of various coherence levels for a random viewing duration. At the onset of a mechanical perturbation that rapidly stretched the pectoralis muscle, they indicated the perceived motion direction by making a reaching movement to one of two targets. Using electromyography (EMG), we quantified the reflex gains of the pectoralis and posterior deltoid muscles. Results show that reflex gains scaled with both the coherence level and the viewing duration of the stimulus. We fit a drift diffusion model (DDM) to the behavioral choices. The decision variable (DV), derived from the DDM, correlated well with the measured reflex gain at the single-trial level. However, when matched on DV magnitude, reflex gains were significantly lower in CoM than non-CoM trials. We conclude that the internal state of the motor system, as measured by the spinal reflexes, reflects the continual deliberation on sensory evidence for action selection, including the postdecisional evidence that can lead to a change of mind.NEW & NOTEWORTHY Using behavioral findings, EMG, and computational modeling, we show that not only the perceptual decision outcome but also the accumulating evidence for that outcome is continuously sent to the relevant muscles. Moreover, we show that an upcoming change of mind can be detected in the motor periphery, suggesting that a correlate of the internal decision making process is being sent along.

Late integration of vision and proprioception during perturbed reaches.

The motor system corrects rapidly, but selectively, for perturbations to ongoing reaching movements, depending on the constraints of the task. To account for such sophistication, it has been postulated that corrections are based on an estimated limb state that integrates all sensory changes caused by the perturbation, taking into account their processing delays. Here, we asked if information from different sensory modalities is integrated immediately or processed separately in the early phase of a response. We perturbed the estimated state of the limb with both unimodal and bimodal visual and proprioceptive perturbations without changing the actual limb state. For visual perturbations, a cursor representing the hand was shifted to the left or the right relative to the true hand location. For proprioceptive perturbations, the biceps or triceps muscles were vibrated, which induced illusory limb-state changes to the right or the left. In the bimodal condition, the perturbations to vision and proprioception were either congruent or incongruent in their directions. Response latencies show that it takes ∼100 ms longer to respond to unimodal visual perturbations than to unimodal proprioceptive perturbations. Responses to bimodal perturbations show that it takes an additional ∼100 ms beyond the response to unimodal visual perturbations for intermodal consistency to impact the response. These results suggest that visual and proprioceptive signals are initially processed separately for state estimation and only combined at the level of the limb's motor output, instead of being immediately integrated into a single state estimate of the limb.NEW & NOTEWORTHY Both visual and proprioceptive signals provide information about arm state during reaching. By perturbing the perceived, but not the actual, position of the hand in both modalities using visual disturbances and muscle vibration, we examined multimodal integration and state estimation during reaching. Our results suggest that the early reach corrections are based on separate state estimates from the two sensory modalities and only later are based on a combined state estimate.

Predictive steering: integration of artificial motor signals in self-motion estimation.

The brain's computations for active and passive self-motion estimation can be unified with a single model that optimally combines vestibular and visual signals with sensory predictions based on efference copies. It is unknown whether this theoretical framework also applies to the integration of artificial motor signals, such as those that occur when driving a car, or whether self-motion estimation in this situation relies on sole feedback control. Here, we examined if training humans to control a self-motion platform leads to the construction of an accurate internal model of the mapping between the steering movement and the vestibular reafference. Participants (n = 15) sat on a linear motion platform and actively controlled the platform's velocity using a steering wheel to translate their body to a memorized visual target (motion condition). We compared their steering behavior to that of participants (n = 15) who remained stationary and instead aligned a nonvisible line with the target (stationary condition). To probe learning, the gain between the steering wheel angle and the platform or line velocity changed abruptly twice during the experiment. These gain changes were virtually undetectable in the displacement error in the motion condition, whereas clear deviations were observed in the stationary condition, showing that participants in the motion condition made within-trial changes to their steering behavior. We conclude that vestibular feedback allows not only the online control of steering but also a rapid adaptation to the gain changes to update the brain's internal model of the mapping between the steering movement and the vestibular reafference.NEW & NOTEWORTHY Perception of self-motion is known to depend on the integration of sensory signals and, when the motion is self-generated, the predicted sensory reafference based on motor efference copies. Here we show, using a closed-loop steering experiment with a direct coupling between the steering movement and the vestibular self-motion feedback, that humans are also able to integrate artificial motor signals, like the motor signals that occur when driving a car.

Assessing corticospinal excitability and reaching hand choice during whole body motion.

Behavioral studies have shown that humans account for inertial acceleration in their decisions of hand choice when reaching during body motion. Physiologically, it is unclear at what stage of movement preparation information about body motion is integrated with the process of hand selection. Here, we addressed this question by applying transcranial magnetic stimulation over left motor cortex (M1) of human participants who performed a preferential reach task while they were sinusoidally translated on a linear motion platform. If M1 only represents a read-out of the final hand choice, we expect the body motion not to affect the motor-evoked potential (MEP) amplitude. If body motion biases the hand selection process before target onset, we expect corticospinal excitability to be influenced by the phase of the motion, with larger MEP amplitudes for phases that show a bias to using the right hand. Behavioral results replicate our earlier findings of a sinusoidal modulation of hand choice bias with motion phase. MEP amplitudes also show a sinusoidal modulation with motion phase, suggesting that body motion influences corticospinal excitability, which may ultimately reflect changes of hand preference. The modulation being present before target onset suggests that competition between hands is represented throughout the corticospinal tract. Its phase relationship with the motion profile indicates that other processes after target onset take up time until the hand selection process has been completely resolved, and the reach is initiated.NEW & NOTEWORTHY Full body-motion biases decisions of hand choice. We examined the signatures of this bias in hand preference in corticospinal excitability before a reach target was presented. Our results show that behavior and corticospinal excitability modulate depending on the state of the body in motion. This suggests that information about body motion penetrates deeply within the motor system.

Age-related reweighting of visual and vestibular cues for vertical perception.

As we age, the acuity of our sensory organs declines, which may affect our lifestyle. Sensory deterioration in the vestibular system is typically bilateral and gradual, and could lead to problems with balance and spatial orientation. To compensate for the sensory deterioration, it has been suggested that the brain reweights the sensory information sources according to their relative noise characteristics. For rehabilitation and training programs, it is important to understand the consequences of this reweighting, preferably at the individual subject level. We psychometrically examined the age-dependent reweighting of visual and vestibular cues used in spatial orientation in a group of 32 subjects (age range: 19-76 yr). We asked subjects to indicate the orientation of a line (clockwise or counterclockwise relative to the gravitational vertical) presented within an oriented square visual frame when seated upright or with their head tilted 30° relative to the body. Results show that subjects' vertical perception is biased by the orientation of the visual frame. Both the magnitude of this bias and response variability become larger with increasing age. Deducing the underlying sensory noise characteristics, using Bayesian inference, suggests an age-dependent reweighting of sensory information, with an increasing weight of the visual contextual information. Further scrutiny of the model suggests that this shift in sensory weights is the result of an increase in the noise of the vestibular signal. Our approach quantifies how noise properties of visual and vestibular systems change over the life span, which helps to understand the aging process at the neurocomputational level. NEW & NOTEWORTHY Perception of visual vertical involves a weighted fusion of visual and vestibular tilt cues. Using a Bayesian approach and experimental psychophysics, we quantify how this fusion process changes with age. We show that, with age, the vestibular information is down-weighted whereas the visual weight is increased. This shift in sensory reweighting is primarily due to an age-related increase of the noise of vestibular signals.

Transformation of vestibular signals for the decisions of hand choice during whole body motion.

In daily life, we frequently reach toward objects while our body is in motion. We have recently shown that body accelerations influence the decision of which hand to use for the reach, possibly by modulating the body-centered computations of the expected reach costs. However, head orientation relative to the body was not manipulated, and hence it remains unclear whether vestibular signals contribute in their head-based sensory frame or in a transformed body-centered reference frame to these cost calculations. To test this, subjects performed a preferential reaching task to targets at various directions while they were sinusoidally translated along the lateral body axis, with their head either aligned with the body (straight ahead) or rotated 18° to the left. As a measure of hand preference, we determined the target direction that resulted in equiprobable right/left-hand choices. Results show that head orientation affects this balanced target angle when the body is stationary but does not further modulate hand preference when the body is in motion. Furthermore, reaction and movement times were larger for reaches to the balanced target angle, resembling a competitive selection process, and were modulated by head orientation when the body was stationary. During body translation, reaction and movement times depended on the phase of the motion, but this phase-dependent modulation had no interaction with head orientation. We conclude that the brain transforms vestibular signals to body-centered coordinates at the early stage of reach planning, when the decision of hand choice is computed. NEW & NOTEWORTHY The brain takes inertial acceleration into account in computing the anticipated biomechanical costs that guide hand selection during whole body motion. Whereas these costs are defined in a body-centered, muscle-based reference frame, the otoliths detect the inertial acceleration in head-centered coordinates. By systematically manipulating head position relative to the body, we show that the brain transforms otolith signals into body-centered coordinates at an early stage of reach planning, i.e., before the decision of hand choice is computed.

Task-dependent responses to muscle vibration during reaching.

Feedback corrections in reaching have been shown to be task-dependent for proprioceptive, visual and vestibular perturbations, in line with predictions from optimal feedback control theory. Mechanical perturbations have been used to elicit proprioceptive errors, but have the drawback to actively alter the limb's trajectory, making it nontrivial to dissociate the subject's compensatory response from the perturbation itself. In contrast, muscle vibration provides an alternative tool to perturb the muscle afferents without changing the hands trajectory, inducing only changes in the estimated, but not the actual, limb position and velocity. Here, we investigate whether upper-arm muscle vibration is sufficient to evoke task-dependent feedback corrections during goal-directed reaching to a narrow versus a wide target. Our main result is that for vibration of biceps and triceps, compensatory responses were down-regulated for the wide compared to the narrow target. The earliest detectable difference between these target-specific corrections is at about 100 ms, likely reflecting a task-dependent feedback control policy rather than a voluntary response.

Visual orientation uncertainty in the rod-and-frame illusion.

Estimation of the orientation of the head relative to the earth's vertical is thought to rely on the integration of vestibular and visual cues. The role of visual cues can be tested using a rod-and-frame task in which a global visual scene, typically a square frame, is displayed at different orientations together with a rod whose perceived direction is a proxy for the head-in-space estimate. While it is known that the frame biases this percept, and hence the subjective visual vertical, the possible role of the rod itself in this processing has not been examined. Current models about spatial orientation assume that the visual orientation of the rod and its uncertainty play no role in the visual-vestibular integration process, but are only involved in the transformation that yields rod orientation in space, thereby contributing additive noise to the subjective visual vertical. Here we tested the validity of this assumption in the rod-and-frame task by replacing the rod with an ellipse whose orientation uncertainty was manipulated by varying its eccentricity (i.e., making the ellipse more or less rounded). Using a psychophysical approach, subjects performed this ellipse-and-frame task for three different eccentricities of the ellipse (0.74, 0.82, 0.99) and three frame orientations (-17.5°, 0°, 17.5°). Results show that ellipse eccentricity affects the uncertainty but not the bias of the subjective visual vertical, suggesting that the ellipse does not interact with the frame in global visual processing but contributes additive noise in computing its orientation in world coordinates.

Reference frames in the decisions of hand choice.

For the brain to decide on a reaching movement, it needs to select which hand to use. A number of body-centered factors affect this decision, such as the anticipated movement costs of each arm, recent choice success, handedness, and task demands. While the position of each hand relative to the target is also known to be an important spatial factor, it is unclear which reference frames coordinate the spatial aspects in the decisions of hand choice. Here we tested the role of gaze- and head-centered reference frames in a hand selection task. With their head and gaze oriented in different directions, we measured hand choice of 19 right-handed subjects instructed to make unimanual reaching movements to targets at various directions relative to their body. Using an adaptive procedure, we determined the target angle that led to equiprobable right/left hand choices. When gaze remained fixed relative to the body this balanced target angle shifted systematically with head orientation, and when head orientation remained fixed this choice measure shifted with gaze. These results suggest that a mixture of head- and gaze-centered reference frames is involved in the spatially guided decisions of hand choice, perhaps to flexibly bind this process to the mechanisms of target selection. NEW & NOTEWORTHY Decisions of target and hand choice are fundamental aspects of human reaching movements. While the reference frames involved in target choice have been identified, it is unclear which reference frames are involved in hand selection. We tested the role of gaze- and head-centered reference frames in a hand selection task. Findings emphasize the role of both spatial reference frames in the decisions of hand choice, in addition to known body-centered computations such anticipated movement costs and handedness.

Corticospinal correlates of fast and slow adaptive processes in motor learning.

Recent computational theories and behavioral observations suggest that motor learning is supported by multiple adaptation processes, operating on different timescales, but direct neural evidence is lacking. We tested this hypothesis by applying transcranial magnetic stimulation over motor cortex in 16 human subjects during a validated reach adaptation task. Motor-evoked potentials (MEPs) and cortical silent periods (CSPs) were recorded from the biceps brachii to assess modulations of corticospinal excitability as indices for corticospinal plasticity. Guided by a two-state adaptation model, we show that the MEP reflects an adaptive process that learns quickly but has poor retention, while the CSP correlates with a process that responds more slowly but retains information well. These results provide a physiological link between models of motor learning and distinct changes in corticospinal excitability. Our findings support the relationship between corticospinal gain modulations and the adaptive processes in motor learning. NEW & NOTEWORTHY Computational theories and behavioral observations suggest that motor learning is supported by multiple adaptation processes, but direct neural evidence is lacking. We tested this hypothesis by applying transcranial magnetic stimulation over human motor cortex during a reach adaptation task. Guided by a two-state adaptation model, we show that the motor-evoked potential reflects a process that adapts and decays quickly, whereas the cortical silent period reflects slow adaptation and decay.

Bayesian quantification of sensory reweighting in a familial bilateral vestibular disorder (DFNA9).

DFNA9 is a rare progressive autosomal dominantly inherited vestibulo-cochlear disorder, resulting in a homogeneous group of patients with hearing impairment and bilateral vestibular function loss. These patients suffer from a deteriorated sense of spatial orientation, leading to balance problems in darkness, especially on irregular surfaces. Both behavioral and functional imaging studies suggest that the remaining sensory cues could compensate for the loss of vestibular information. A thorough model-based quantification of this reweighting in individual patients is, however, missing. Here we psychometrically examined the individual patient's sensory reweighting of these cues after complete vestibular loss. We asked a group of DFNA9 patients and healthy control subjects to judge the orientation (clockwise or counterclockwise relative to gravity) of a rod presented within an oriented square frame (rod-in-frame task) in three different head-on-body tilt conditions. Our results show a cyclical frame-induced bias in perceived gravity direction across a 90° range of frame orientations. The magnitude of this bias was significantly increased in the patients compared with the healthy control subjects. Response variability, which increased with head-on-body tilt, was also larger for the patients. Reverse engineering of the underlying signal properties, using Bayesian inference principles, suggests a reweighting of sensory signals, with an increase in visual weight of 20-40% in the patients. Our approach of combining psychophysics and Bayesian reverse engineering is the first to quantify the weights associated with the different sensory modalities at an individual patient level, which could make it possible to develop personal rehabilitation programs based on the patient's sensory weight distribution. NEW & NOTEWORTHY It has been suggested that patients with vestibular deficits can compensate for this loss by increasing reliance on other sensory cues, although an actual quantification of this reweighting is lacking. We combine experimental psychophysics with a reverse engineering approach based on Bayesian inference principles to quantify sensory reweighting in individual vestibular patients. We discuss the suitability of this approach for developing personal rehabilitation programs based on the patient's sensory weight distribution.

Bayesian adaptive stimulus selection for dissociating models of psychophysical data.

Comparing models facilitates testing different hypotheses regarding the computational basis of perception and action. Effective model comparison requires stimuli for which models make different predictions. Typically, experiments use a predetermined set of stimuli or sample stimuli randomly. Both methods have limitations; a predetermined set may not contain stimuli that dissociate the models, whereas random sampling may be inefficient. To overcome these limitations, we expanded the psi-algorithm (Kontsevich & Tyler, 1999) from estimating the parameters of a psychometric curve to distinguishing models. To test our algorithm, we applied it to two distinct problems. First, we investigated dissociating sensory noise models. We simulated ideal observers with different noise models performing a two-alternative forced-choice task. Stimuli were selected randomly or using our algorithm. We found using our algorithm improved the accuracy of model comparison. We also validated the algorithm in subjects by inferring which noise model underlies speed perception. Our algorithm converged quickly to the model previously proposed (Stocker & Simoncelli, 2006), whereas if stimuli were selected randomly, model probabilities separated slower and sometimes supported alternative models. Second, we applied our algorithm to a different problem-comparing models of target selection under body acceleration. Previous work found target choice preference is modulated by whole body acceleration (Rincon-Gonzalez et al., 2016). However, the effect is subtle, making model comparison difficult. We show that selecting stimuli adaptively could have led to stronger conclusions in model comparison. We conclude that our technique is more efficient and more reliable than current methods of stimulus selection for dissociating models.

Task-dependent vestibular feedback responses in reaching.

When reaching for an earth-fixed object during self-rotation, the motor system should appropriately integrate vestibular signals and sensory predictions to compensate for the intervening motion and its induced inertial forces. While it is well established that this integration occurs rapidly, it is unknown whether vestibular feedback is specifically processed dependent on the behavioral goal. Here, we studied whether vestibular signals evoke fixed responses with the aim to preserve the hand trajectory in space or are processed more flexibly, correcting trajectories only in task-relevant spatial dimensions. We used galvanic vestibular stimulation to perturb reaching movements toward a narrow or a wide target. Results show that the same vestibular stimulation led to smaller trajectory corrections to the wide than the narrow target. We interpret this reduced compensation as a task-dependent modulation of vestibular feedback responses, tuned to minimally intervene with the task-irrelevant dimension of the reach. These task-dependent vestibular feedback corrections are in accordance with a central prediction of optimal feedback control theory and mirror the sophistication seen in feedback responses to mechanical and visual perturbations of the upper limb.NEW & NOTEWORTHY Correcting limb movements for external perturbations is a hallmark of flexible sensorimotor behavior. While visual and mechanical perturbations are corrected in a task-dependent manner, it is unclear whether a vestibular perturbation, naturally arising when the body moves, is selectively processed in reach control. We show, using galvanic vestibular stimulation, that reach corrections to vestibular perturbations are task dependent, consistent with a prediction of optimal feedback control theory.

Decisions in motion: passive body acceleration modulates hand choice.

In everyday life, we frequently have to decide which hand to use for a certain action. It has been suggested that for this decision the brain calculates expected costs based on action values, such as expected biomechanical costs, expected success rate, handedness, and skillfulness. Although these conclusions were based on experiments in stationary subjects, we often act while the body is in motion. We investigated how hand choice is affected by passive body motion, which directly affects the biomechanical costs of the arm movement due to its inertia. With the use of a linear motion platform, 12 right-handed subjects were sinusoidally translated (0.625 and 0.5 Hz). At 8 possible motion phases, they had to reach, using either their left or right hand, to a target presented at 1 of 11 possible locations. We predicted hand choice by calculating the expected biomechanical costs under different assumptions about the future acceleration involved in these computations, being the forthcoming acceleration during the reach, the instantaneous acceleration at target onset, or zero acceleration as if the body were stationary. Although hand choice was generally biased to use of the dominant hand, it also modulated sinusoidally with the motion, with the amplitude of the bias depending on the motion's peak acceleration. The phase of hand choice modulation was consistent with the cost model that took the instantaneous acceleration signal at target onset. This suggests that the brain relies on the bottom-up acceleration signals, and not on predictions about future accelerations, when deciding on hand choice during passive whole body motion.NEW & NOTEWORTHY Decisions of hand choice are a fundamental aspect of human behavior. Whereas these decisions are typically studied in stationary subjects, this study examines hand choice while subjects are in motion. We show that accelerations of the body, which differentially modulate the biomechanical costs of left and right hand movements, are also taken into account when deciding which hand to use for a reach, possibly based on bottom-up processing of the otolith signal.

Dissociating vestibular and somatosensory contributions to spatial orientation.

Inferring object orientation in the surroundings heavily depends on our internal sense of direction of gravity. Previous research showed that this sense is based on the integration of multiple information sources, including visual, vestibular (otolithic), and somatosensory signals. The individual noise characteristics and contributions of these sensors can be studied using spatial orientation tasks, such as the subjective visual vertical (SVV) task. A recent study reported that patients with complete bilateral vestibular loss perform similar as healthy controls on these tasks, from which it was conjectured that the noise levels of both otoliths and body somatosensors are roll-tilt dependent. Here, we tested this hypothesis in 10 healthy human subjects by roll tilting the head relative to the body to dissociate tilt-angle dependencies of otolith and somatosensory noise. Using a psychometric approach, we measured the perceived orientation, and its variability, of a briefly flashed line relative to the gravitational vertical (SVV). Measurements were taken at multiple body-in-space orientations (-90 to 90°, steps of 30°) and head-on-body roll tilts (30° left ear down, aligned, 30° right ear down). Results showed that verticality perception is processed in a head-in-space reference frame, with a systematic SVV error that increased with larger head-in-space orientations. Variability patterns indicated a larger contribution of the otolith organs around upright and a more substantial contribution of the body somatosensors at larger body-in-space roll tilts. Simulations show that these findings are consistent with a statistical model that involves tilt-dependent noise levels of both otolith and somatosensory signals, confirming dynamic shifts in the weights of sensory inputs with tilt angle.

Deliberation in the motor system: reflex gains track evolving evidence leading to a decision.

Both decision making and sensorimotor control require real-time processing of noisy information streams. Historically these processes were thought to operate sequentially: cognitive processing leads to a decision, and the outcome is passed to the motor system to be converted into action. Recently, it has been suggested that the decision process may provide a continuous flow of information to the motor system, allowing it to prepare in a graded fashion for the probable outcome. Such continuous flow is supported by electrophysiology in nonhuman primates. Here we provide direct evidence for the continuous flow of an evolving decision variable to the motor system in humans. Subjects viewed a dynamic random dot display and were asked to indicate their decision about direction by moving a handle to one of two targets. We probed the state of the motor system by perturbing the arm at random times during decision formation. Reflex gains were modulated by the strength and duration of motion, reflecting the accumulated evidence in support of the evolving decision. The magnitude and variance of these gains tracked a decision variable that explained the subject's decision accuracy. The findings support a continuous process linking the evolving computations associated with decision making and sensorimotor control.

Noise in the nervous system.

Noise--random disturbances of signals--poses a fundamental problem for information processing and affects all aspects of nervous-system function. However, the nature, amount and impact of noise in the nervous system have only recently been addressed in a quantitative manner. Experimental and computational methods have shown that multiple noise sources contribute to cellular and behavioural trial-to-trial variability. We review the sources of noise in the nervous system, from the molecular to the behavioural level, and show how noise contributes to trial-to-trial variability. We highlight how noise affects neuronal networks and the principles the nervous system applies to counter detrimental effects of noise, and briefly discuss noise's potential benefits.