Noise in the nervous system Faisal, A. Aldo; Selen, Luc P. J; Wolpert, Daniel M
Nature reviews. Neuroscience,
04/2008, Letnik:
9, Številka:
4
Journal Article
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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.
When we reach for an object during a passive whole body rotation, a tangential Coriolis force is generated on the arm. Yet, within a few trials, the brain adapts to this force so it does not disrupt ...the reach. Is this adaptation governed by a single-rate or dual-rate learning process? Here, guided by state-space modeling, we studied human reach adaptation in a fully-enclosed rotating room. After 90 pre-rotation reaches (baseline), participants were trained to make 240 to-and-fro reaches while the room rotated at 10 rpm (block A), then performed 6 reaches under opposite room rotation (block B), and subsequently made 100 post-rotation reaches (washout). A control group performed the same paradigm, but without the reaches during rotation block B. Single-rate and dual-rate models can be best dissociated if there would be full un-learning of compensation A during block B, but minimal learning of B. From the perspective of a dual-rate model, the un-learning observed in block B would mainly be caused by the faster state, such that the washout reaches would show retention effects of the slower state, called spontaneous recovery. Alternatively, following a single-rate model, the same state would govern the learning in block A and un-learning in block B, such that the washout reaches mimic the baseline reaches. Our results do not provide clear signs of spontaneous recovery in the washout reaches. Model fits further show that a single-rate process outperformed a dual-rate process. We suggest that a single-rate process underlies Coriolis force reach adaptation, perhaps because these forces relate to familiar body dynamics and are assigned to an internal cause.
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.
Many sensorimotor activities have a time constraint for successful completion. In this case, any time devoted to sensory processing is at the expense of time available for motor execution. Earlier ...studies have explored how this competition between sensory processing and motor execution is resolved by using experimental designs that segregate the sensing and acting phase of the task. It was found that participants switch from the sensing to the acting stage such that the overall (sensorimotor) uncertainty in the outcome of the task is minimized. An unexplained observation in these studies is the substantial variability in switching times. We investigated the variability in switching time by correlating it with the underlying sensorimotor uncertainty. To this end, we used a modified version of the virtual ball catching paradigm proposed by Faisal & Wolpert (2009). Subjects were instructed to catch a ball, but as soon as they initiated their movement the ball disappeared. We extended the range of horizontal velocities and used two different start positions of the ball to quantify the dependence of sensory uncertainty on ball velocity. Velocity dependence of sensory uncertainty allowed us to manipulate sensory uncertainty and hence the sensorimotor uncertainty. We found that the variability in switching times is correlated with two factors. Firstly, variability in switching times is greater when variation in switching time has only minimal effects on sensorimotor uncertainty. Secondly, variability in switching times is greater when the sensorimotor uncertainty is larger. Our results suggest that the variability in switching time reflects an uncertainty-driven exploratory process.
When navigating through the environment, our brain needs to infer how far we move and in which direction we are heading. In this estimation process, the brain may rely on multiple sensory modalities, ...including the visual and vestibular systems. Previous research has mainly focused on heading estimation, showing that sensory cues are combined by weighting them in proportion to their reliability, consistent with statistically optimal integration. But while heading estimation could improve with the ongoing motion, due to the constant flow of information, the estimate of how far we move requires the integration of sensory information across the whole displacement. In this study, we investigate whether the brain optimally combines visual and vestibular information during a displacement estimation task, even if their reliability varies from trial to trial. Participants were seated on a linear sled, immersed in a stereoscopic virtual reality environment. They were subjected to a passive linear motion involving visual and vestibular cues with different levels of visual coherence to change relative cue reliability and with cue discrepancies to test relative cue weighting. Participants performed a two-interval two-alternative forced-choice task, indicating which of two sequentially perceived displacements was larger. Our results show that humans adapt their weighting of visual and vestibular information from trial to trial in proportion to their reliability. These results provide evidence that humans optimally integrate visual and vestibular information in order to estimate their body displacement.
There is ample evidence that humans are able to control the endpoint impedance of their arms in response to active destabilizing force fields. However, such fields are uncommon in daily life. Here, ...we examine whether the CNS selectively controls the endpoint impedance of the arm in the absence of active force fields but in the presence of instability arising from task geometry and signal-dependent noise (SDN) in the neuromuscular system. Subjects were required to generate forces, in two orthogonal directions, onto four differently curved rigid objects simulated by a robotic manipulandum. The endpoint stiffness of the limb was estimated for each object curvature. With increasing curvature, the endpoint stiffness increased mainly parallel to the object surface and to a lesser extent in the orthogonal direction. Therefore, the orientation of the stiffness ellipses did not orient to the direction of instability. Simulations showed that the observed stiffness geometries and their pattern of change with instability are the result of a tradeoff between maximizing the mechanical stability and minimizing the destabilizing effects of SDN. Therefore, it would have been suboptimal to align the stiffness ellipse in the direction of instability. The time course of the changes in stiffness geometry suggests that modulation takes place both within and across trials. Our results show that an increase in stiffness relative to the increase in noise can be sufficient to reduce kinematic variability, thereby allowing stiffness control to improve stability in natural tasks.
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.
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.
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.
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.
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.
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