scholarly journals Individuals with cerebellar degeneration show similar adaptation deficits with large and small visuomotor errors

2013 ◽  
Vol 109 (4) ◽  
pp. 1164-1173 ◽  
Author(s):  
John E. Schlerf ◽  
Jing Xu ◽  
Nola M. Klemfuss ◽  
Thomas L. Griffiths ◽  
Richard B. Ivry
Keyword(s):  
Sensory Information ◽  
External Perturbation ◽  
Visuomotor Adaptation ◽  
Error Signal ◽  
Credit Assignment ◽  
Visuomotor Rotation ◽  
Motor Variability ◽  
Large Step ◽  
The Difference ◽  
Computational Analyses

The cerebellum has long been recognized to play an important role in motor adaptation. Individuals with cerebellar ataxia exhibit impaired learning in visuomotor adaptation tasks such as prism adaptation and force field learning. Both types of tasks involve the adjustment of an internal model to compensate for an external perturbation. This updating process is error driven, with the error signal based on the difference between anticipated and actual sensory information. This process may entail a credit assignment problem, with a distinction made between error arising from faulty representation of the environment and error arising from noise in the controller. We hypothesized that people with ataxia may perform poorly at visuomotor adaptation because they attribute a greater proportion of their error to their motor control difficulties. We tested this hypothesis using a computational model based on a Kalman filter. We imposed a 20-deg visuomotor rotation in either a single large step or in a series of smaller 5-deg steps. The ataxic group exhibited a comparable deficit in both conditions. The computational analyses indicate that the patients' deficit cannot be accounted for simply by their increased motor variability. Rather, the patients' deficit in learning may be related to difficulty in estimating the instability in the environment or variability in their motor system.

The Synergistic Organization of Muscle Recruitment Constrains Visuomotor Adaptation

2009 ◽  
Vol 101 (5) ◽  
pp. 2263-2269 ◽  
Author(s):  
Aymar de Rugy ◽  
Mark R. Hinder ◽  
Daniel G. Woolley ◽  
Richard G. Carson
Keyword(s):  
Time Course ◽  
Neural Circuits ◽  
Visual Target ◽  
Sensory Information ◽  
Visuomotor Adaptation ◽  
Visuomotor Rotation ◽  
Joint Torques ◽  
Flexion Extension ◽  
Isometric Torque ◽  
The Individual

Reaching to visual targets engages the nervous system in a series of transformations between sensory information and motor commands. That which remains to be determined is the extent to which the processes that mediate sensorimotor adaptation to novel environments engage neural circuits that represent the required movement in joint-based or muscle-based coordinate systems. We sought to establish the contribution of these alternative representations to the process of visuomotor adaptation. To do so we applied a visuomotor rotation during a center-out isometric torque production task that involved flexion/extension and supination/pronation at the elbow-joint complex. In separate sessions, distinct half-quadrant rotations (i.e., 45°) were applied such that adaptation could be achieved either by only rescaling the individual joint torques (i.e., the visual target and torque target remained in the same quadrant) or by additionally requiring torque reversal at a contributing joint (i.e., the visual target and torque target were in different quadrants). Analysis of the time course of directional errors revealed that the degree of adaptation was lower (by ∼20%) when reversals in the direction of joint torques were required. It has been established previously that in this task space, a transition between supination and pronation requires the engagement of a different set of muscle synergists, whereas in a transition between flexion and extension no such change is required. The additional observation that the initial level of adaptation was lower and the subsequent aftereffects were smaller, for trials that involved a pronation–supination transition than for those that involved a flexion–extension transition, supports the conclusion that the process of adaptation engaged, at least in part, neural circuits that represent the required motor output in a muscle-based coordinate system.

scholarly journals The Effect of Visual Uncertainty on Implicit Motor Adaptation

2020 ◽  
Author(s):  
Jonathan S. Tsay ◽  
Guy Avraham ◽  
Hyosub E. Kim ◽  
Darius E. Parvin ◽  
Zixuan Wang ◽  
...  
Keyword(s):  
Alternative Hypothesis ◽  
Visuomotor Adaptation ◽  
Modular System ◽  
Feedback Signal ◽  
Sensorimotor Adaptation ◽  
Prediction Errors ◽  
Error Signal ◽  
The Difference ◽  
Visual Error ◽  
Sensorimotor Map

ABSTRACTSensorimotor adaptation is driven by sensory prediction errors, the difference between the predicted and actual feedback. When the position of the feedback is made uncertain, adaptation is attenuated. This effect, in the context of optimal sensory integration models, has been attributed to a weakening of the error signal driving adaptation. Here we consider an alternative hypothesis, namely that uncertainty alters the perceived location of the feedback. We present two visuomotor adaptation experiments to compare these hypotheses, varying the size and uncertainty of a visual error signal. Uncertainty attenuated learning when the error size was small but had no effect when the error size was large. This pattern of results favors the hypothesis that uncertainty does not impact the strength of the error signal, but rather, leads to mis-localization of the error. We formalize these ideas to offer a novel perspective on the effect of visual uncertainty on implicit sensorimotor adaptation.SIGNIFICANCE STATEMENTCurrent models of sensorimotor adaptation assume that the rate of learning will be related to properties of the error signal (e.g., size, consistency, relevance). Recent evidence has challenged this view, pointing to a rigid, modular system, one that automatically recalibrates the sensorimotor map in response to movement errors, with minimal constraint. In light of these developments, this study revisits the influence of feedback uncertainty on sensorimotor adaptation. Adaptation was attenuated in response to a noisy feedback signal, but the effect was only manifest for small errors and not for large errors. This interaction suggests that uncertainty does not weaken the error signal. Rather, it may influence the perceived location of the feedback and thus the change in the sensorimotor map induced by that error. These ideas are formalized to show how the motor system remains exquisitely calibrated, even if adaptation is largely insensitive to the statistics of error signals.

Adjustable set point: to honor Harold T. Hammel

2006 ◽  
Vol 100 (4) ◽  
pp. 1338-1346 ◽  
Author(s):  
Michel Cabanac
Keyword(s):  
Temperature Regulation ◽  
Structural Characteristics ◽  
External Perturbation ◽  
External Signal ◽  
Error Signal ◽  
Internal Temperature ◽  
Set Point ◽  
Actual Temperature ◽  
Information Input ◽  
The Difference

The value of a regulated variable in the absence of external perturbation stabilizes at the set point of the system. This set point is an information input that may be determined by an external signal to which the regulated variable is compared or may be determined by the structural characteristics of the system itself. In the case of temperature regulation the actual internal temperature is compared with the set point “wanted” by the organism. The activating signal for the regulatory responses, the “error signal,” is the difference between the actual temperature and the set point. When an error signal is detected, the organism produces the available corrective responses. Yet, the notion of thermoregulatory set point has been challenged recently. Such a questioning entails that both fever and anapyrexia are useless concepts. This minireview examines the available arguments and data and concludes that to abandon the concepts of set point, fever, and anapyrexia is premature, at best.

Neural Processing of Gravito-Inertial Cues in Humans. IV. Influence of Visual Rotational Cues During Roll Optokinetic Stimuli

2003 ◽  
Vol 89 (1) ◽  
pp. 390-400 ◽  
Author(s):  
L. H. Zupan ◽  
D. M. Merfeld
Keyword(s):  
Visual Cues ◽  
Gravitational Force ◽  
Sensory Information ◽  
Inertial Force ◽  
Linear Acceleration ◽  
Otolith Organs ◽  
Optokinetic Stimulation ◽  
The Difference ◽  
The Right ◽  
Roll Tilt

Sensory systems often provide ambiguous information. For example, otolith organs measure gravito-inertial force (GIF), the sum of gravitational force and inertial force due to linear acceleration. However, according to Einstein's equivalence principle, a change in gravitational force due to tilt is indistinguishable from a change in inertial force due to translation. Therefore the central nervous system (CNS) must use other sensory cues to distinguish tilt from translation. For example, the CNS might use dynamic visual cues indicating rotation to help determine the orientation of gravity (tilt). This, in turn, might influence the neural processes that estimate linear acceleration, since the CNS might estimate gravity and linear acceleration such that the difference between these estimates matches the measured GIF. Depending on specific sensory information inflow, inaccurate estimates of gravity and linear acceleration can occur. Specifically, we predict that illusory tilt caused by roll optokinetic cues should lead to a horizontal vestibuloocular reflex compensatory for an interaural estimate of linear acceleration, even in the absence of actual linear acceleration. To investigate these predictions, we measured eye movements binocularly using infrared video methods in 17 subjects during and after optokinetic stimulation about the subject's nasooccipital (roll) axis (60°/s, clockwise or counterclockwise). The optokinetic stimulation was applied for 60 s followed by 30 s in darkness. We simultaneously measured subjective roll tilt using a somatosensory bar. Each subject was tested in three different orientations: upright, pitched forward 10°, and pitched backward 10°. Five subjects reported significant subjective roll tilt (>10°) in directions consistent with the direction of the optokinetic stimulation. In addition to torsional optokinetic nystagmus and afternystagmus, we measured a horizontal nystagmus to the right during and following clockwise (CW) stimulation and to the left during and following counterclockwise (CCW) stimulation. These measurements match predictions that subjective tilt in the absence of real tilt should induce a nonzero estimate of interaural linear acceleration and, therefore, a horizontal eye response. Furthermore, as predicted, the horizontal response in the dark was larger for Tilters ( n = 5) than for Non-Tilters ( n= 12).

scholarly journals Can patients with cerebellar disease switch learning mechanisms to reduce their adaptation deficits?

Brain ◽  
2019 ◽  
Vol 142 (3) ◽  
pp. 662-673 ◽  
Author(s):  
Aaron L Wong ◽  
Cherie L Marvel ◽  
Jordan A Taylor ◽  
John W Krakauer
Keyword(s):  
Prediction Error ◽  
Poor Performance ◽  
Visuomotor Adaptation ◽  
Cerebellar Degeneration ◽  
Prediction Errors ◽  
Cerebellar Disease ◽  
Learning Mechanisms ◽  
Visuomotor Rotation ◽  
Age Related ◽  
Sensory Prediction

Abstract Systematic perturbations in motor adaptation tasks are primarily countered by learning from sensory-prediction errors, with secondary contributions from other learning processes. Despite the availability of these additional processes, particularly the use of explicit re-aiming to counteract observed target errors, patients with cerebellar degeneration are surprisingly unable to compensate for their sensory-prediction error deficits by spontaneously switching to another learning mechanism. We hypothesized that if the nature of the task was changed—by allowing vision of the hand, which eliminates sensory-prediction errors—patients could be induced to preferentially adopt aiming strategies to solve visuomotor rotations. To test this, we first developed a novel visuomotor rotation paradigm that provides participants with vision of their hand in addition to the cursor, effectively setting the sensory-prediction error signal to zero. We demonstrated in younger healthy control subjects that this promotes a switch to strategic re-aiming based on target errors. We then showed that with vision of the hand, patients with cerebellar degeneration could also switch to an aiming strategy in response to visuomotor rotations, performing similarly to age-matched participants (older controls). Moreover, patients could retrieve their learned aiming solution after vision of the hand was removed (although they could not improve beyond what they retrieved), and retain it for at least 1 year. Both patients and older controls, however, exhibited impaired overall adaptation performance compared to younger healthy controls (age 18–33 years), likely due to age-related reductions in spatial and working memory. Patients also failed to generalize, i.e. they were unable to adopt analogous aiming strategies in response to novel rotations. Hence, there appears to be an inescapable obligatory dependence on sensory-prediction error-based learning—even when this system is impaired in patients with cerebellar disease. The persistence of sensory-prediction error-based learning effectively suppresses a switch to target error-based learning, which perhaps explains the unexpectedly poor performance by patients with cerebellar degeneration in visuomotor adaptation tasks.

scholarly journals Trial-by-trial analysis of intermanual transfer during visuomotor adaptation

2011 ◽  
Vol 106 (6) ◽  
pp. 3157-3172 ◽  
Author(s):  
Jordan A. Taylor ◽  
Greg J. Wojaczynski ◽  
Richard B. Ivry
Keyword(s):  
Skill Acquisition ◽  
Training Transfer ◽  
Visuomotor Adaptation ◽  
Single Step ◽  
Hand Movements ◽  
Intermanual Transfer ◽  
Visuomotor Rotation ◽  
Left Hand ◽  
Right Hand ◽  
The Right

Studies of intermanual transfer have been used to probe representations formed during skill acquisition. We employ a new method that provides a continuous assay of intermanual transfer, intermixing right- and left-hand trials while limiting visual feedback to right-hand movements. We manipulated the degree of awareness of the visuomotor rotation, introducing a 22.5° perturbation in either an abrupt single step or gradually in ∼1° increments every 10 trials. Intermanual transfer was observed with the direction of left-hand movements shifting in the opposite direction of the rotation over the course of training. The transfer on left-hand trials was less than that observed in the right hand. Moreover, the magnitude of transfer was larger in our mixed-limb design compared with the standard blocked design in which transfer is only probed at the end of training. Transfer was similar in the abrupt and gradual groups, suggesting that awareness of the perturbation has little effect on intermanual transfer. In a final experiment, participants were provided with a strategy to offset an abrupt rotation, a method that has been shown to increase error over the course of training due to the operation of sensorimotor adaptation. This deterioration was also observed on left-hand probe trials, providing further support that awareness has little effect on intermanual transfer. These results indicate that intermanual transfer is not dependent on the implementation of cognitively assisted strategies that participants might adopt when they become aware that the visuomotor mapping has been perturbed. Rather, the results indicate that the information available to processes involved in adaptation entails some degree of effector independence.

scholarly journals Feature attention for binocular disparity in primate area MT depends on tuning strength

2015 ◽  
Vol 113 (5) ◽  
pp. 1545-1555 ◽  
Author(s):  
Douglas A. Ruff ◽  
Richard T. Born
Keyword(s):  
Binocular Disparity ◽  
Receptive Fields ◽  
Sensory Information ◽  
Neuronal Population ◽  
Area Mt ◽  
Temporal Area ◽  
Mt Neurons ◽  
Feature Attention ◽  
The Difference ◽  
The Relationship

Attending to a stimulus modulates the responses of sensory neurons that represent features of that stimulus, a phenomenon named “feature attention.” For example, attending to a stimulus containing upward motion enhances the responses of upward-preferring direction-selective neurons in the middle temporal area (MT) and suppresses the responses of downward-preferring neurons, even when the attended stimulus is outside of the spatial receptive fields of the recorded neurons (Treue S, Martinez-Trujillo JC. Nature 399: 575–579, 1999). This modulation renders the representation of sensory information across a neuronal population more selective for the features present in the attended stimulus (Martinez-Trujillo JC, Treue S. Curr Biol 14: 744–751, 2004). We hypothesized that if feature attention modulates neurons according to their tuning preferences, it should also be sensitive to their tuning strength, which is the magnitude of the difference in responses to preferred and null stimuli. We measured how the effects of feature attention on MT neurons in rhesus monkeys ( Macaca mulatta) depended on the relationship between features—in our case, direction of motion and binocular disparity—of the attended stimulus and a neuron's tuning for those features. We found that, as for direction, attention to stimuli containing binocular disparity cues modulated the responses of MT neurons and that the magnitude of the modulation depended on both a neuron's tuning preferences and its tuning strength. Our results suggest that modulation by feature attention may depend not just on which features a neuron represents but also on how well the neuron represents those features.

scholarly journals Explaining Savings for Visuomotor Adaptation: Linear Time-Invariant State-Space Models Are Not Sufficient

2008 ◽  
Vol 100 (5) ◽  
pp. 2537-2548 ◽  
Author(s):  
Eric Zarahn ◽  
Gregory D. Weston ◽  
Johnny Liang ◽  
Pietro Mazzoni ◽  
John W. Krakauer
Keyword(s):  
State Space ◽  
Linear Time ◽  
State Space Model ◽  
Visuomotor Adaptation ◽  
Invariant State ◽  
Visuomotor Rotation ◽  
Body Memory ◽  
Linear Time Invariant ◽  
And Coping ◽  
Time Invariant

Adaptation of the motor system to sensorimotor perturbations is a type of learning relevant for tool use and coping with an ever-changing body. Memory for motor adaptation can take the form of savings: an increase in the apparent rate constant of readaptation compared with that of initial adaptation. The assessment of savings is simplified if the sensory errors a subject experiences at the beginning of initial adaptation and the beginning of readaptation are the same. This can be accomplished by introducing either 1) a sufficiently small number of counterperturbation trials (counterperturbation paradigm [ CP]) or 2) a sufficiently large number of zero-perturbation trials (washout paradigm [ WO]) between initial adaptation and readaptation. A two-rate, linear time-invariant state-space model (SSMLTI,2) was recently shown to theoretically produce savings for CP. However, we reasoned from superposition that this model would be unable to explain savings for WO. Using the same task (planar reaching) and type of perturbation (visuomotor rotation), we found comparable savings for both CP and WO paradigms. Although SSMLTI,2 explained some degree of savings for CP it failed completely for WO. We conclude that for visuomotor rotation, savings in general is not simply a consequence of LTI dynamics. Instead savings for visuomotor rotation involves metalearning, which we show can be modeled as changes in system parameters across the phases of an adaptation experiment.

scholarly journals Similarities Between Somatosensory Cortical Responses Induced via Natural Touch and Microstimulation in the Ventral Posterior Lateral Thalamus in Macaques

2021 ◽  
Author(s):  
Joseph T Francis ◽  
Anna Rozenboym ◽  
Lee von Kraus ◽  
Shaohua Xu ◽  
Pratik Chhatbar ◽  
...  
Keyword(s):  
Somatosensory System ◽  
Sensory Information ◽  
Rodent Model ◽  
Robotic Arm ◽  
Neural Responses ◽  
Sensory Stimuli ◽  
Thalamic Stimulation ◽  
Cortical Responses ◽  
The Difference ◽  
Sensory Neural

Lost sensations, such as touch, could be restored by microstimulation (MiSt) along the sensory neural substrate. Such neuroprosthetic sensory information can be used as feedback from an invasive brain-machine interface (BMI) to control a robotic arm/hand, such that tactile and proprioceptive feedback from the sensorized robotic arm/hand is directly given to the BMI user. Microstimulation in the human somatosensory thalamus (Vc) has been shown to produce somatosensory perceptions. However, until recently, systematic methods for using thalamic stimulation to evoke naturalistic touch perceptions were lacking. We have recently presented rigorous methods for determining a mapping between ventral posterior lateral thalamus (VPL) MiSt, and neural responses in the somatosensory cortex (S1), in a rodent model (Choi et al., 2016; Choi and Francis, 2018). Our technique minimizes the difference between S1 neural responses induced by natural sensory stimuli and those generated via VPL MiSt. Our goal is to develop systems that know what MiSt will produce a given neural response and possibly a more natural "sensation." To date, our optimization has been conducted in the rodent model and simulations. Here we present data from simple non-optimized thalamic MiSt during peri-operative experiments, where we MiSt in the VPL of macaques with a somatosensory system more like humans. We implanted arrays of microelectrodes across the hand area of the macaque S1 cortex as well as in the VPL thalamus. Multi and single-unit recordings were used to compare cortical responses to natural touch and thalamic MiSt in the anesthetized state. Post stimulus time histograms were highly correlated between the VPL MiSt and natural touch modalities, adding support to the use of VPL MiSt towards producing a somatosensory neuroprosthesis in humans.

scholarly journals Sensitivity to Error During Visuomotor Adaptation is Similarly Modulated by Abrupt, Gradual and Random Perturbation Schedules

2021 ◽  
Author(s):  
Susan Coltman ◽  
Robert J. van Beers ◽  
Pieter W Medendorp ◽  
Paul Gribble
Keyword(s):  
Random Perturbation ◽  
Visuomotor Adaptation ◽  
Learning Processes ◽  
Control Group ◽  
Initial Training ◽  
Prior Learning ◽  
Visuomotor Rotation ◽  
Learning Groups ◽  
Error Sensitivity ◽  
Slow Learning

It has been suggested that sensorimotor adaptation involves at least two processes (i.e., fast and slow) that differ in retention and error sensitivity. Previous work has shown that repeated exposure to an abrupt force field perturbation results in greater error sensitivity for both the fast and slow processes. While this implies that the faster relearning is associated with increased error sensitivity, it remains unclear what aspects of prior experience modulate error sensitivity. In the present study, we manipulated the initial training using different perturbation schedules, thought to differentially affect fast and slow learning processes based on error magnitude, and then observed what effect prior learning had on subsequent adaptation. During initial training of a visuomotor rotation task, we exposed three groups of participants to either an abrupt, a gradual, or a random perturbation schedule. During a testing session, all three groups were subsequently exposed to an abrupt perturbation schedule. Comparing the two sessions of the control group who experienced repetition of the same perturbation, we found an increased error sensitivity for both processes. We found that the error sensitivity was increased for both the fast and slow processes, with no reliable changes in the retention, for both the gradual and structural learning groups when compared to the first session of the control group. We discuss the findings in the context of how fast and slow learning processes respond to a history of errors.

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