Dynamics of dual prism adaptation: relating novel experimental results to a minimalistic neural model.
ABSTRACT: In everyday life, humans interact with a dynamic environment often requiring rapid adaptation of visual perception and motor control. In particular, new visuo-motor mappings must be learned while old skills have to be kept, such that after adaptation, subjects may be able to quickly change between two different modes of generating movements ('dual-adaptation'). A fundamental question is how the adaptation schedule determines the acquisition speed of new skills. Given a fixed number of movements in two different environments, will dual-adaptation be faster if switches ('phase changes') between the environments occur more frequently? We investigated the dynamics of dual-adaptation under different training schedules in a virtual pointing experiment. Surprisingly, we found that acquisition speed of dual visuo-motor mappings in a pointing task is largely independent of the number of phase changes. Next, we studied the neuronal mechanisms underlying this result and other key phenomena of dual-adaptation by relating model simulations to experimental data. We propose a simple and yet biologically plausible neural model consisting of a spatial mapping from an input layer to a pointing angle which is subjected to a global gain modulation. Adaptation is performed by reinforcement learning on the model parameters. Despite its simplicity, the model provides a unifying account for a broad range of experimental data: It quantitatively reproduced the learning rates in dual-adaptation experiments for both direct effect, i.e. adaptation to prisms, and aftereffect, i.e. behavior after removal of prisms, and their independence on the number of phase changes. Several other phenomena, e.g. initial pointing errors that are far smaller than the induced optical shift, were also captured. Moreover, the underlying mechanisms, a local adaptation of a spatial mapping and a global adaptation of a gain factor, explained asymmetric spatial transfer and generalization of prism adaptation, as observed in other experiments.
Project description:Prism adaptation (PA) is both a perceptual-motor learning task as well as a promising rehabilitation tool for visuo-spatial neglect (VSN)-a spatial attention disorder often experienced after stroke resulting in slowed and/or inaccurate motor responses to contralesional targets. During PA, individuals are exposed to prism-induced shifts of the visual-field while performing a visuo-guided reaching task. After adaptation, with goggles removed, visuomotor responding is shifted to the opposite direction of that initially induced by the prisms. This visuomotor aftereffect has been used to study visuomotor learning and adaptation and has been applied clinically to reduce VSN severity by improving motor responding to stimuli in contralesional (usually left-sided) space. In order to optimize PA's use for VSN patients, it is important to elucidate the neural and cognitive processes that alter visuomotor function during PA. In the present study, healthy young adults underwent PA while event-related potentials (ERPs) were recorded at the termination of each reach (screen-touch), then binned according to accuracy (hit vs. miss) and phase of exposure block (early, middle, late). Results show that two ERP components were evoked by screen-touch: an error-related negativity (ERN), and a P300. The ERN was consistently evoked on miss trials during adaptation, while the P300 amplitude was largest during the early phase of adaptation for both hit and miss trials. This study provides evidence of two neural signals sensitive to visual feedback during PA that may sub-serve changes in visuomotor responding. Prior ERP research suggests that the ERN reflects an error processing system in medial-frontal cortex, while the P300 is suggested to reflect a system for context updating and learning. Future research is needed to elucidate the role of these ERP components in improving visuomotor responses among individuals with VSN.
Project description:During the procedure of prism adaptation, subjects execute pointing movements to visual targets under a lateral optical displacement: as consequence of the discrepancy between visual and proprioceptive inputs, their visuo-motor activity is characterized by pointing errors. The perception of such final errors triggers error-correction processes that eventually result into sensori-motor compensation, opposite to the prismatic displacement (i.e., after-effects). Here we tested whether the mere observation of erroneous pointing movements, similar to those executed during prism adaptation, is sufficient to produce adaptation-like after-effects. Neurotypical participants observed, from a first-person perspective, the examiner's arm making incorrect pointing movements that systematically overshot visual targets location to the right, thus simulating a rightward optical deviation. Three classical after-effect measures (proprioceptive, visual and visual-proprioceptive shift) were recorded before and after first-person's perspective observation of pointing errors. Results showed that mere visual exposure to an arm that systematically points on the right-side of a target (i.e., without error correction) produces a leftward after-effect, which mostly affects the observer's proprioceptive estimation of her body midline. In addition, being exposed to such a constant visual error induced in the observer the illusion "to feel" the seen movement. These findings indicate that it is possible to elicit sensori-motor after-effects by mere observation of movement errors.
Project description:Movements toward an object displaced optically through prisms adapt quickly, a striking example for the plasticity of neuronal visuomotor programs. We investigated the degree and time course of this system's plasticity. Participants performed goal-directed throwing or pointing movements with terminal feedback before, during, and after wearing prism goggles shifting the visual world laterally either to the right or to the left. Prism adaptation was incomplete even after 240 throwing movements, still deviating significantly laterally by on average of 0.8° (CI?=?0.20°) at the end of the adaptation period. The remaining lateral deviation was significant for pointing movements only with left shifting prisms. In both tasks, removal of the prisms led to an aftereffect which disappeared in the course of further training. This incomplete prism adaptation may be caused by movement variability combined with an adaptive neuronal control system exhibiting a finite capacity for evaluating movement errors.
Project description:Peripheral prisms (p-prisms) shift peripheral portions of the visual field of one eye, providing visual field expansion for patients with hemianopia. However, patients rarely show adaption to the shift, incorrectly localizing objects viewed within the p-prisms. A pilot evaluation of a novel computerized perceptual-motor training program aiming to promote p-prism adaption was conducted.Thirteen patients with hemianopia fitted with 57? oblique p-prisms completed the training protocol. They attended six 1-hour visits reaching and touching peripheral checkerboard stimuli presented over videos of driving scenes while fixating a central target. Performance was measured at each visit and after 3 months.There was a significant reduction in touch error (P = 0.01) for p-prism zone stimuli from pretraining median of 16.6° (IQR 12.1°-19.6°) to 2.7° ( IQR 1.0°-8.5°) at the end of training. P-prism zone reaction times did not change significantly with training (P > 0.05). P-prism zone detection improved significantly (P = 0.01) from a pretraining median 70% (IQR 50%-88%) to 95% at the end of training (IQR 73%-98%). Three months after training improvements had regressed but performance was still better than pretraining.Improved pointing accuracy for stimuli detected in prism-expanded vision of patients with hemianopia wearing 57? oblique p-prisms is possible and training appears to further improve detection.This is the first use of this novel software to train adaptation of visual direction in patients with hemianopia wearing peripheral prisms.
Project description:Cognitive demands for postural control increase with aging and cognitive-motor interference (CMI) exists for a number of walking situations, especially with visuo-spatial cognitive tasks. Such interference also influences spatial learning abilities among older adults; however, this is rarely considered in research on aging in spatial navigation. We posited that visually and physically exploring an unknown environment may be subject to CMI for older adults. We investigated potential indicators of postural control interfering with spatial learning. Given known associations between age-related alterations in gait and brain structure, we also examined potential neuroanatomical correlates of this interference. Fourteen young and 14 older adults had to find an invisible goal in an unfamiliar, real, ecological environment. We measured walking speed, trajectory efficiency (direct route over taken route) and goal fixations (proportion of visual fixations toward the goal area). We calculated the change in walking speed between the first and last trials and adaptation indices for all three variables to quantify their modulation across learning trials. All participants were screened with a battery of visuo-cognitive tests. Eighteen of our participants (10 young, 8 older) also underwent a magnetic resonance imaging (MRI) examination. Older adults reduced their walking speed considerably on the first, compared to the last trial. The adaptation index of walking speed correlated positively with those of trajectory efficiency and goal fixations, indicating a reduction in resource sharing between walking and encoding the environment. The change in walking speed correlated negatively with gray matter volume in superior parietal and occipital regions and the precuneus. We interpret older adults' change in walking speed as indicative of CMI, similar to dual task costs. This is supported by the correlations between the adaptation indices and between the change in walking speed and gray matter volume in brain regions that are important for navigation, given that they are involved in visual attention, sensory integration and encoding of space. These findings under ecological conditions in a natural spatial learning task question what constitutes dual tasking in older adults and they can lead future research to reconsider the actual cognitive burden of postural control in aging navigation research.
Project description:Humans can learn and store multiple visuomotor mappings (dual-adaptation) when feedback for each is provided alternately. Moreover, learned context cues associated with each mapping can be used to switch between the stored mappings. However, little is known about the associative learning between cue and required visuomotor mapping, and how learning generalises to novel but similar conditions. To investigate these questions, participants performed a rapid target-pointing task while we manipulated the offset between visual feedback and movement end-points. The visual feedback was presented with horizontal offsets of different amounts, dependent on the targets shape. Participants thus needed to use different visuomotor mappings between target location and required motor response depending on the target shape in order to "hit" it. The target shapes were taken from a continuous set of shapes, morphed between spiky and circular shapes. After training we tested participants performance, without feedback, on different target shapes that had not been learned previously. We compared two hypotheses. First, we hypothesised that participants could (explicitly) extract the linear relationship between target shape and visuomotor mapping and generalise accordingly. Second, using previous findings of visuomotor learning, we developed a (implicit) Bayesian learning model that predicts generalisation that is more consistent with categorisation (i.e. use one mapping or the other). The experimental results show that, although learning the associations requires explicit awareness of the cues' role, participants apply the mapping corresponding to the trained shape that is most similar to the current one, consistent with the Bayesian learning model. Furthermore, the Bayesian learning model predicts that learning should slow down with increased numbers of training pairs, which was confirmed by the present results. In short, we found a good correspondence between the Bayesian learning model and the empirical results indicating that this model poses a possible mechanism for simultaneously learning multiple visuomotor mappings.
Project description:The human ability to use different tools demonstrates our capability of forming and maintaining multiple, context-specific motor memories. Experimentally, this has been investigated in dual adaptation, where participants adjust their reaching movements to opposing visuomotor transformations. Adaptation in these paradigms occurs by distinct processes, such as strategies for each transformation or the implicit acquisition of distinct visuomotor mappings. Although distinct, transformation-dependent aftereffects have been interpreted as support for the latter, they could reflect adaptation of a single visuomotor map, which is locally adjusted in different regions of the workspace. Indeed, recent studies suggest that explicit aiming strategies direct where in the workspace implicit adaptation occurs, thus potentially serving as a cue to enable dual adaptation. Disentangling these possibilities is critical to understanding how humans acquire and maintain motor memories for different skills and tools. We therefore investigated generalization of explicit and implicit adaptation to untrained movement directions after participants practiced two opposing cursor rotations, which were associated with the visual display being presented in the left or right half of the screen. Whereas participants learned to compensate for opposing rotations by explicit strategies specific to this visual workspace cue, aftereffects were not cue sensitive. Instead, aftereffects displayed bimodal generalization patterns that appeared to reflect locally limited learning of both transformations. By varying target arrangements and instructions, we show that these patterns are consistent with implicit adaptation that generalizes locally around movement plans associated with opposing visuomotor transformations. Our findings show that strategies can shape implicit adaptation in a complex manner. NEW & NOTEWORTHY Visuomotor dual adaptation experiments have identified contextual cues that enable learning of separate visuomotor mappings, but the underlying representations of learning are unclear. We report that visual workspace separation as a contextual cue enables the compensation of opposing cursor rotations by a combination of explicit and implicit processes: Learners developed context-dependent explicit aiming strategies, whereas an implicit visuomotor map represented dual adaptation independent from arbitrary context cues by local adaptation around the explicit movement plan.
Project description:Hemispatial neglect ('neglect') is a disabling condition that can follow damage to the right side of the brain, in which patients show difficulty in responding to or orienting towards objects and events that occur on the left side of space. Symptoms of neglect can manifest in both space- and object-based frames of reference. Although patients can show a combination of these two forms of neglect, they are considered separable and have distinct neurological bases. In recent years considerable evidence has emerged to demonstrate that spatial symptoms of neglect can be reduced by an intervention called prism adaptation. Patients point towards objects viewed through prismatic lenses that shift the visual image to the right. Approximately five minutes of repeated pointing results in a leftward recalibration of pointing and improved performance on standard clinical tests for neglect. The understanding of prism adaptation has also been advanced through studies of healthy participants, in whom adaptation to leftward prismatic shifts results in temporary neglect-like performance. Here we examined the effect of prism adaptation on the performance of healthy participants who completed a computerised test of space- and object-based attention. Participants underwent adaptation to leftward- or rightward-shifting prisms, or performed neutral pointing according to a between-groups design. Significant pointing after-effects were found for both prism groups, indicating successful adaptation. In addition, the results of the computerised test revealed larger reaction-time costs associated with shifts of attention between two objects compared to shifts of attention within the same object, replicating previous work. However there were no differences in the performance of the three groups, indicating that prism adaptation did not influence space- or object-based attention for this task. When combined with existing literature, the results are consistent with the proposal that prism adaptation may only perturb cognitive functions for which normal baseline performance is already biased.
Project description:In many laboratory visuo-motor decision tasks, subjects compensate for their own visuo-motor error, earning close to the maximum reward possible. To do so, they must combine information about the distribution of possible error with values associated with different movement outcomes. The optimal solution is a potentially difficult computation that presupposes knowledge of the probability density function (pdf) of visuo-motor error associated with each possible planned movement. It is unclear how the brain represents such pdfs or computes with them. In three experiments, we used a forced-choice method to reveal subjects' internal representations of their spatial visuo-motor error in a speeded reaching movement. Although subjects' objective distributions were unimodal, close to Gaussian, their estimated internal pdfs were typically multimodal and were better described as mixtures of a small number of distributions differing only in location and scale. Mixtures of a small number of uniform distributions outperformed other mixture distributions, including mixtures of Gaussians.
Project description:Prisms laterally shifting the perceived visual world cause arm movements to deviate from intended targets. The resulting error-the direct effect-both for pointing and throwing movements, usually corresponds to only around half of the prism's optical power due to an "immediate correction effect". We investigated the mechanisms of this immediate correction effect. In three experiments with 73 healthy subjects we find that the immediate correction effect is associated with a head and/or eye rotation. Since these rotations are subconscious they are not taken into account by the participants. These subconscious rotations compensate for a large portion of the prism's optical effect and change the subjective straight ahead. These movements seem to be induced only in a rich visual environment and hence do not take place in the dark. They correspond to the difference between the direct effect and the optical power of the prisms and seem to cause the immediate correction effect. Hence, eye-hand adaptation only adapts to the prism's optical power minus unconscious head rotation and hence is much smaller than the optical power of the prisms.