scholarly journals Visuomotor learning from postdictive motor error

eLife ◽  
2021 ◽  
Vol 10 ◽  
Author(s):  
Jana Masselink ◽  
Markus Lappe

Sensorimotor learning adapts motor output to maintain movement accuracy. For saccadic eye movements, learning also alters space perception, suggesting a dissociation between the performed saccade and its internal representation derived from corollary discharge (CD). This is critical since learning is commonly believed to be driven by CD-based visual prediction error. We estimate the internal saccade representation through pre- and trans-saccadic target localization, showing that it decouples from the actual saccade during learning. We present a model that explains motor and perceptual changes by collective plasticity of spatial target percept, motor command, and a forward dynamics model that transforms CD from motor into visuospatial coordinates. We show that learning does not follow visual prediction error but instead a postdictive update of space after saccade landing. We conclude that trans-saccadic space perception guides motor learning via CD-based postdiction of motor error under the assumption of a stable world.

2021 ◽  
Vol 11 (1) ◽  
Author(s):  
Daniel H. Blustein ◽  
Ahmed W. Shehata ◽  
Erin S. Kuylenstierna ◽  
Kevin B. Englehart ◽  
Jonathon W. Sensinger

AbstractWhen a person makes a movement, a motor error is typically observed that then drives motor planning corrections on subsequent movements. This error correction, quantified as a trial-by-trial adaptation rate, provides insight into how the nervous system is operating, particularly regarding how much confidence a person places in different sources of information such as sensory feedback or motor command reproducibility. Traditional analysis has required carefully controlled laboratory conditions such as the application of perturbations or error clamping, limiting the usefulness of motor analysis in clinical and everyday environments. Here we focus on error adaptation during unperturbed and naturalistic movements. With increasing motor noise, we show that the conventional estimation of trial-by-trial adaptation increases, a counterintuitive finding that is the consequence of systematic bias in the estimate due to noise masking the learner’s intention. We present an analytic solution relying on stochastic signal processing to reduce this effect of noise, producing an estimate of motor adaptation with reduced bias. The result is an improved estimate of trial-by-trial adaptation in a human learner compared to conventional methods. We demonstrate the effectiveness of the new method in analyzing simulated and empirical movement data under different noise conditions.


2002 ◽  
Vol 87 (2) ◽  
pp. 679-695 ◽  
Author(s):  
Robijanto Soetedjo ◽  
Chris R. S. Kaneko ◽  
Albert F. Fuchs

There is general agreement that saccades are guided to their targets by means of a motor error signal, which is produced by a local feedback circuit that calculates the difference between desired saccadic amplitude and an internal copy of actual saccadic amplitude. Although the superior colliculus (SC) is thought to provide the desired saccadic amplitude signal, it is unclear whether the SC resides in the feedback loop. To test this possibility, we injected muscimol into the brain stem region containing omnipause neurons (OPNs) to slow saccades and then determined whether the firing of neurons at different sites in the SC was altered. In 14 experiments, we produced saccadic slowing while simultaneously recording the activity of a single SC neuron. Eleven of the 14 neurons were saccade-related burst neurons (SRBNs), which discharged their most vigorous burst for saccades with an optimal amplitude and direction (optimal vector). The optimal directions for the 11 SRBNs ranged from nearly horizontal to nearly vertical, with optimal amplitudes between 4 and 17°. Although muscimol injections into the OPN region produced little change in the optimal vector, they did increase mean saccade duration by 25 to 192.8% and decrease mean saccade peak velocity by 20.5 to 69.8%. For optimal vector saccades, both the acceleration and deceleration phases increased in duration. However, during 10 of 14 experiments, the duration of deceleration increased as fast as or faster than that of acceleration as saccade duration increased, indicating that most of the increase in duration occurred during the deceleration phase. SRBNs in the SC changed their burst duration and firing rate concomitantly with changes in saccadic duration and velocity, respectively. All SRBNs showed a robust increase in burst duration as saccadic duration increased. Five of 11 SRBNs also exhibited a decrease in burst peak firing rate as saccadic velocity decreased. On average across the neurons, the number of spikes in the burst was constant. There was no consistent change in the discharge of the three SC neurons that did not exhibit bursts with saccades. Our data show that the SC receives feedback from downstream saccade-related neurons about the ongoing saccades. However, the changes in SC firing produced in our study do not suggest that the feedback is involved with producing motor error. Instead, the feedback seems to be involved with regulating the duration of the discharge of SRBNs so that the desired saccadic amplitude signal remains present throughout the saccade.


2018 ◽  
Author(s):  
Kremer Yves ◽  
Flakowski Jérôme ◽  
Rohner Clément ◽  
Lüscher Christian

AbstractDopamine (DA) neurons of the ventral tegmental area (VTA) track external cues and rewards to generate a reward prediction error (RPE) signal during Pavlovian conditioning. Here we explored how RPE is implemented for a self-paced, operant task in freely moving mice. The animal could trigger a reward-predicting cue by remaining in a specific location of an operant box for a brief time before moving to a spout for reward collection. In vivo single-unit recordings revealed phasic responses to the cue and reward in correct trials, while with failures the activity paused, reflecting positive and negative error signals of a reward prediction. In addition, a majority of VTA DA neurons also encoded parameters of the goal-directed action (e.g. movement velocity, acceleration, distance to goal and licking) by changes in tonic firing rate. Such multiplexing of individual neurons was only apparent while the mouse was engaged in the task. We conclude that a multiplexed internal representation during the task modulates VTA DA neuron activity, indicating a multimodal prediction error that shapes behavioral adaptation of a self-paced goal-directed action.


2006 ◽  
Vol 9 (2) ◽  
pp. 312-320 ◽  
Author(s):  
Alessandra Ackel Rodrigues ◽  
Susi Lippi Marques

Studies of visual space perception have been assuming that people have an internal representation of the physical space that surrounds them. A variety of psychophysical procedures has been used in an attempt to measure the properties of visual space. The goal of the present study was to evaluate the accuracy of the mental representation and the strategies adopted to acquire and retain visuo-spatial information of a configuration as a function of two types of instructions. Thirty-eight undergraduate and graduate students participated in the study and were distributed in perceptive and mnemonic experimental conditions. The effect of the instructions (intentional and incidental) on the representation of the distances among the objects of the scene was estimated using exponents of power function, based on the reproduction of the distances among the stimuli of the scene. The results revealed that judgments made under intentional instructions were more frequently based on strategies related to the location of the stimuli, whereas judgments originating from incidental instructions were based on strategies related to the name of the stimuli. It was observed that the intentional instruction facilitated a more accurate mental representation of the observed experimental configuration, enhancing participants' performance.


2021 ◽  
Author(s):  
Jonathan Tsay ◽  
Adrian Haith ◽  
Richard B Ivry ◽  
Hyosub E Kim

While sensory-prediction error (SPE), the difference between predicted and actual sensory feedback, is recognized as the primary signal that drives implicit motor recalibration, recent studies have shown that task error (TE), the difference between sensory feedback and the movement goal, also plays a modulatory role. To systematically examine how SPE and TE collectively shape implicit recalibration, we performed a series of visuomotor learning experiments, introducing perturbations that varied the size of TE using a popular target displacement method and the size of SPE using a clamped visual feedback method. In Experiments 1 & 2, we observed robust sign-dependent changes in hand angle in response to perturbations with both SPE and TE but failed to observe changes in hand angle in response to TE-only perturbations. Yet in Experiments 3 & 4, the magnitude of TE modulated implicit recalibration in the presence of a fixed SPE. Taken together, these results underscore that implicit recalibration is driven by both SPE and TE (Kim, Parvin, & Ivry, 2019), while specifying unappreciated interactions between these two error-based processes. First, TE only impacts implicit calibration when SPE is present. Second, transient changes occurring when the target is displaced to manipulate TE has an attenuating effect on implicit recalibration, perhaps due to attention being directed away from the sensory feedback.


1990 ◽  
Vol 64 (2) ◽  
pp. 509-531 ◽  
Author(s):  
D. Guitton ◽  
D. P. Munoz ◽  
H. L. Galiana

1. Orienting movements, consisting of coordinated eye and head displacements, direct the visual axis to the source of a sensory stimulus. A recent hypothesis suggests that the CNS may control gaze position (gaze = eye-relative-to-space = eye-relative-to-head + head-relative-to-space) by the use of a feedback circuit wherein an internally derived representation of gaze motor error drives both eye and head premotor circuits. In this paper we examine the effect of behavioral task on the individual and summed trajectories of horizontal eye- and head-orienting movements to gain more insight into how the eyes and head are coupled and controlled in different behavioral situations. 2. Cats whose heads were either restrained (head-fixed) or unrestrained (head-free) were trained to make orienting movements of any desired amplitude in a simple cat-and-mouse game we call the barrier paradigm. A rectangular opaque barrier was placed in front of the hungry animal who either oriented to a food target that was visible to one side of the barrier or oriented to a location on an edge of the barrier where it predicted the target would reappear from behind the barrier. 3. The dynamics (e.g., maximum velocity) and duration of eye- and head-orienting movements were affected by the task. Saccadic eye movements (head-fixed) elicited by the visible target attained greater velocity and had shorter durations than comparable amplitude saccades directed toward the predicted target. A similar observation has been made in human and monkey. In addition, when the head was unrestrained both the eye and head movements (and therefore gaze movements) were faster and shorter in the visible- compared with the predicted-target conditions. Nevertheless, the relative contributions of the eye and head to the overall gaze displacement remained task independent: i.e., the distance traveled by the eye and head movements was determined by the size of the gaze shift only. This relationship was maintained because the velocities of the eye and head movements covaried in the different behavioral situations. Gaze-velocity profiles also had characteristic shapes that were dependent on task. In the predicted-target condition these profiles tended to have flattened peaks, whereas when the target was visible the peaks were sharper. 4. Presentation of a visual cue (e.g., reappearance of food target) immediately before (less than 50 ms) the onset of a gaze shift to a predicted target triggered a midflight increase in first the eye- and, after approximately 20 ms, the head-movement velocity.(ABSTRACT TRUNCATED AT 400 WORDS)


1994 ◽  
Vol 72 (6) ◽  
pp. 2754-2770 ◽  
Author(s):  
E. L. Keller ◽  
J. A. Edelman

1. We recorded the spatial and temporal dynamics of saccade-related burst neurons (SRBNs) found in the intermediate layers of the superior colliculus (SC) in the alert, behaving monkey. These burst cells are normally the first neurons recorded during radially directed microelectrode penetrations of the SC after the electrode has left the more dorsally situated visual layers. They have spatially delimited movement fields whose centers describe the well-studied motor map of the SC. They have a rather sharp, saccade-locked burst of activity that peaks just before saccade onset and then declines steeply during the saccade. Many of these cells, when recorded during saccade trials, also have an early, transient visual response and an irregular prelude of presaccadic activity. 2. Because saccadic eye movements normally have very stereotyped durations and velocity trajectories that vary systematically with saccade size, it has been difficult in the past to establish quantitatively whether the activity of SRBNs temporally codes dynamic saccadic control signals, e.g., dynamic motor error or eye velocity, where dynamic motor error is defined as a signal proportional to the instantaneous difference between desired final eye position and the actual eye position during a saccade. It has also not been unequivocally established whether SRBNs participate in an organized spatial shift of ensemble activity in the intermediate layers of the SC during saccadic eye movements. 3. To address these issues, we studied the activity of SRBNs using an interrupted saccade paradigm. Saccades were interrupted with pulsatile electrical stimulation through a microelectrode implanted in the omnipauser region of the brain stem while recordings were made simultaneously from single SRBNs in the SC. 4. Shortly after the beginning of the stimulation (which was electronically triggered at saccade onset), the eyes decelerated rapidly and stopped completely. When the high-frequency (typically 300-400 pulses per second) stimulation was terminated (average duration 12 ms), the eye movement was reinitiated and a resumed saccade was made accurately to the location of the target. 5. When we recorded from SRBNs in the more caudal colliculus, which were active for large saccades, cell discharge was powerfully and rapidly suppressed by the stimulation (average latency = 3.8 ms). Activity in the same cells started again just before the onset of the resumed saccade and continued during this saccade even though it has a much smaller amplitude than would normally be associated with significant discharge for caudal SC cells.(ABSTRACT TRUNCATED AT 400 WORDS)


1986 ◽  
Vol 66 (1) ◽  
pp. 118-171 ◽  
Author(s):  
D. L. Sparks

Afferent signals that guide orienting movements converge in the deeper layers of the SC in a wide variety of animals. The sensory cells are arranged topographically according to their receptive-field locations and, thereby, form maps of sensory space. Maps of visual, somatosensory, and/or auditory space have been obtained in the iguana, mouse, hamster, barn owl, chinchilla, cat, and monkey. The deeper layers of the SC also contain neurons involved in the generation of movements of the eyes, head, vibrissae, and pinnae. Thus the SC, a site containing multiple sensory maps and perhaps multiple motor maps, has been selected by many investigators as a structure for investigating the problem of sensorimotor integration. In the mammalian nervous system, emphasized in this review, much remains to be learned about the structure, organization, and function of the SC. While anatomical studies continue to add to the knowledge of the sources of afferent projections, their pattern of laminar termination, and the source and destination of efferent projections, relatively little is known about the intrinsic organization of the colliculus, especially the deeper layers. Recently, electrophysiological studies have moved from an emphasis on the sensory and motor properties of collicular neurons to an examination of the maps of auditory and somatosensory space and the correspondence of these maps. In the future, major efforts aimed at identifying the functional properties of cells that project to the SC from diverse brain regions as well as the functional properties that project to the various structures receiving input from the colliculus are needed. A combination of anatomical and electrophysiological methods is required to describe the signal transforms that occur between the SC and motor areas (such as the paramedian pontine reticular formation) closer to the final common pathway. Conceptual and empirical work is needed to develop and test models of how the dynamic visual and auditory maps found in the primate SC are generated. In general, new and/or improved models of the role of the SC in sensorimotor integration are needed as guides for future research. A point of view emphasized here is that it may be fruitful to examine the function of the SC from a motor perspective. The nature of the motor command imposes constraints on the configuration of signals that can initiate movements and thereby determines the required transformation of sensory signals.


2016 ◽  
Vol 6 (1) ◽  
Author(s):  
Rahim Malekshahi ◽  
Anil Seth ◽  
Amalia Papanikolaou ◽  
Zenon Mathews ◽  
Niels Birbaumer ◽  
...  

Abstract Emerging evidence indicates that prediction, instantiated at different perceptual levels, facilitate visual processing and enable prompt and appropriate reactions. Until now, the mechanisms underlying the effect of predictive coding at different stages of visual processing have still remained unclear. Here, we aimed to investigate early and late processing of spatial prediction violation by performing combined recordings of saccadic eye movements and fast event-related fMRI during a continuous visual detection task. Psychophysical reverse correlation analysis revealed that the degree of mismatch between current perceptual input and prior expectations is mainly processed at late rather than early stage, which is instead responsible for fast but general prediction error detection. Furthermore, our results suggest that conscious late detection of deviant stimuli is elicited by the assessment of prediction error’s extent more than by prediction error per se. Functional MRI and functional connectivity data analyses indicated that higher-level brain systems interactions modulate conscious detection of prediction error through top-down processes for the analysis of its representational content, and possibly regulate subsequent adaptation of predictive models. Overall, our experimental paradigm allowed to dissect explicit from implicit behavioral and neural responses to deviant stimuli in terms of their reliance on predictive models.


1988 ◽  
Vol 1 (2) ◽  
pp. 239-244 ◽  
Author(s):  
James T. McIlwain

AbstractThe trajectories of saccadic eye movements evoked electrically from many brain structures are dependent to some degree on the initial position of the eye. Under certain conditions, likely to occur in stimulation experiments, local feedback models of the saccadic system can yield eye movements which behave in this way. The models in question assume that an early processing stage adds an internal representation of eye position to retinal error to yield a signal representing target position with respect to the head. The saccadic system is driven by the difference between this signal and one representing the current position of the eye. Albano & Wurtz (1982) pointed out that lesions perturbing the computation of eye position with respect to the head can result in initial position dependence of visually evoked saccades. It is shown here that position-dependent saccades will also result if electrical stimulation evokes a signal equivalent to retinal error but fails to effect a complete addition of eye position to this signal. Also, when multiple or staircase saccades are produced, as during long stimulus trains, they will have identical directions but decrease progressively in amplitude by a factor related to the fraction of added eye position.


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