Visuomotor Experience Research Articles

Loss of action-related function and connectivity in the blind extrastriate body area.

The Extrastriate Body Area (EBA) participates in the visual perception and motor actions of body parts. We recently showed that EBA's perceptual function develops independently of visual experience, responding to stimuli with body-part information in a supramodal fashion. However, it is still unclear if the EBA similarly maintains its action-related function. Here, we used fMRI to study motor-evoked responses and connectivity patterns in the congenitally blind brain. We found that, unlike the case of perception, EBA does not develop an action-related response without visual experience. In addition, we show that congenital blindness alters EBA's connectivity profile in a counterintuitive way-functional connectivity with sensorimotor cortices dramatically decreases, whereas connectivity with perception-related visual occipital cortices remains high. To the best of our knowledge, we show for the first time that action-related functions and connectivity in the visual cortex could be contingent on visuomotor experience. We further discuss the role of the EBA within the context of visuomotor control and predictive coding theory.

Recalibrating vision-for-action requires years after sight restoration from congenital cataracts.

Being able to perform adept goal-directed actions requires predictive, feed-forward control, including a mapping between the visually estimated target locations and the motor commands reaching for them. When the mapping is perturbed, e.g., due to muscle fatigue or optical distortions, we are quickly able to recalibrate the sensorimotor system to update this mapping. Here, we investigated whether early visual and visuomotor experience is essential for developing sensorimotor recalibration. To this end, we assessed young individuals deprived of pattern vision due to dense congenital bilateral cataracts who were surgically treated for sight restoration only years after birth. We compared their recalibration performance to such distortion to that of age-matched sighted controls. Their sensorimotor recalibration performance was impaired right after surgery. This finding cannot be explained by their still lower visual acuity alone, since blurring vision in controls to a matching degree did not lead to comparable behavior. Nevertheless, the recalibration ability of cataract-treated participants gradually improved with time after surgery. Thus, the lack of early pattern vision affects visuomotor recalibration. However, this ability is not lost but slowly develops after sight restoration, highlighting the importance of sensorimotor experience gained late in life.

Extended visuomotor experience with inverted movements can overcome the inversion effect in biological motion perception

Studies have demonstrated that perceiving human and animal movements as point-light displays is effortless. However, simply inverting the display can significantly impair this ability. Compared to non-dancers and typical dancers, vertical dancers have the unique experience of observing and performing movements upside down as being suspended in the air. We studied whether this unique visuomotor experience makes them better at perceiving the inverted movements. We presented ten pairs of dance movements as point-light displays. Each pair included a version performed on the ground whereas the other was in the air. We inverted the display in half of the trials and asked vertical dancers, typical dancers, and non-dancers about whether the display was inverted. We found that only vertical dancers, who have extended visual and motor experience with the configural and dynamic information of the movements, could identify the inversion of movements performed in the air. Neither typical dancers nor non-dancers, who have no motor experience with performing the inverted movements, could detect the inversion. Our findings suggest that motor experience plays a more critical role in enabling the observers to use dynamic information for identifying artificial inversion in biological motion.

NMDA receptors in visual cortex are necessary for normal visuomotor integration and skill learning.

The experience of coupling between motor output and visual feedback is necessary for the development of visuomotor skills and shapes visuomotor integration in visual cortex. Whether these experience-dependent changes of responses in V1 depend on modifications of the local circuit or are the consequence of circuit changes outside of V1 remains unclear. Here, we probed the role of N-methyl-d-aspartate (NMDA) receptor-dependent signaling, which is known to be involved in neuronal plasticity, in mouse primary visual cortex (V1) during visuomotor development. We used a local knockout of NMDA receptors and a photoactivatable inhibition of CaMKII in V1 during the first visual experience to probe for changes in neuronal activity in V1 as well as the influence on performance in a visuomotor task. We found that a knockout of NMDA receptors before, but not after, first visuomotor experience reduced responses to unpredictable stimuli, diminished the suppression of predictable feedback in V1, and impaired visuomotor skill learning later in life. Our results demonstrate that NMDA receptor-dependent signaling in V1 is critical during the first visuomotor experience for shaping visuomotor integration and enabling visuomotor skill learning.

The Effect of Sport Practice on Enhanced Cognitive Processing of Bodily Indices: A Study on Volleyball Players and Their Ability to Predict Hand Gestures.

To program proper reactions, athletes must anticipate opponents’ actions on the basis of previous visuomotor experience. In particular, such abilities seem to rely on processing others’ intentions to act. We adopted a new approach based on an attentional spatial compatibility paradigm to investigate how elite volleyball players elaborate both spatial and motor information at upper-limb posture presentation. Forty-two participants (18 volleyball players and 17 nonathlete controls assigned to Experiments 1 a and b, and eight basketball players assigned to Experiment 2) were tested to study their ability to process the intentions to act conveyed by hands and extract motor primitives (i.e., significant components of body movements). Analysis looked for a spatial compatibility effect between direction of the spike action (correspondence factor) and response side for both palm and back of the hand (view factor). We demonstrated that volleyball players encoded spatial sport-related indices from bodily information and showed preparatory motor activation according to the direction of the implied spike actions for the palm view (Experiment 1; hand simulating a cross-court spike, p = 0.013, and a down-the-line spike, p = 0.026) but both nonathlete controls (Experiment 1; both p < 0.05) and other sports athletes (basketball players, Experiment 2; p = 0.34, only cross-court spike) did not. Results confirm that elite players’ supremacy lies in the predictive abilities of coding elementary motor primitives for their sport discipline.

Visuomotor Coupling Shapes the Functional Development of Mouse Visual Cortex

The emergence of sensory-guided behavior depends on sensorimotor coupling during development. How sensorimotor experience shapes neural processing is unclear. Here, we show that the coupling between motor output and visual feedback is necessary for the functional development of visual processing in layer 2/3 (L2/3) of primary visual cortex (V1) of the mouse. Using a virtual reality system, we reared mice in conditions of normal or random visuomotor coupling. We recorded the activity of identified excitatory and inhibitory L2/3 neurons in response to transient visuomotor mismatches in both groups of mice. Mismatch responses in excitatory neurons were strongly experience dependent and driven by a transient release from inhibition mediated by somatostatin-positive interneurons. These data are consistent with a model in which L2/3 of V1 computes a difference between an inhibitory visual input and an excitatory locomotion-related input, where the balance between these two inputs is finely tuned by visuomotor experience.

Baby steps: investigating the development of perceptual-motor couplings in infancy.

There are cells in our motor cortex that fire both when we perform and when we observe similar actions. It has been suggested that these perceptual-motor couplings in the brain develop through associative learning during correlated sensorimotor experience. Although studies with adult participants have provided support for this hypothesis, there is no direct evidence that associative learning also underlies the initial formation of perceptual–motor couplings in the developing brain. With the present study we addressed this question by manipulating infants’ opportunities to associate the visual and motor representation of a novel action, and by investigating how this influenced their sensorimotor cortex activation when they observed this action performed by others. Pre-walking 7–9-month-old infants performed stepping movements on an infant treadmill while they either observed their own real-time leg movements (Contingent group) or the previously recorded leg movements of another infant (Non-contingent control group). Infants in a second control group did not perform any steps and only received visual experience with the stepping actions. Before and after the training period we measured infants’ sensorimotor alpha suppression, as an index of sensorimotor cortex activation, while they watched videos of other infants’ stepping actions. While we did not find greater sensorimotor alpha suppression following training in the Contingent group as a whole, we nevertheless found that the strength of the visuomotor contingency experienced during training predicted the amount of sensorimotor alpha suppression at post-test in this group. We did not find any effects of motor experience alone. These results suggest that the development of perceptual–motor couplings in the infant brain is likely to be supported by associative learning during correlated visuomotor experience.

Experience-Enabled Enhancement of Adult Visual Cortex Function

We previously reported in adult mice that visuomotor experience during monocular deprivation (MD) augmented enhancement of visual-cortex-dependent behavior through the non-deprived eye (NDE) during deprivation, and enabled enhanced function to persist after MD. We investigated the physiological substrates of this experience-enabled form of adult cortical plasticity by measuring visual behavior and visually evoked potentials (VEPs) in binocular visual cortex of the same mice before, during, and after MD. MD on its own potentiated VEPs contralateral to the NDE during MD and shifted ocular dominance (OD) in favor of the NDE in both hemispheres. Whereas we expected visuomotor experience during MD to augment these effects, instead enhanced responses contralateral to the NDE, and the OD shift ipsilateral to the NDE were attenuated. However, in the same animals, we measured NMDA receptor-dependent VEP potentiation ipsilateral to the NDE during MD, which persisted after MD. The results indicate that visuomotor experience during adult MD leads to enduring enhancement of behavioral function, not simply by amplifying MD-induced changes in cortical OD, but through an independent process of increasing NDE drive in ipsilateral visual cortex. Because the plasticity is resident in the mature visual cortex and selectively effects gain of visual behavior through experiential means, it may have the therapeutic potential to target and non-invasively treat eye- or visual-field-specific cortical impairment.

Perceptual Judgments of Sports Officials are Influenced by their Motor and Visual Experience

We examined the relation between previous motor and visual experience and current officiating experience of expert judges and referees and their judgments from an embodied cognition viewpoint. A total of 370 sports officials from soccer, handball, ice hockey, and trampoline took part in the study. Analyses revealed that cognitive judgments are related to motor, visual, and officiating experience to different degrees in the analyzed sports. Our findings indicate that, depending on the sport, sports officials should either specialize early in officiating, or gather visuo-motor experience as an athlete or spectator first, and then switch roles to become a sports official.

Neuroimaging reveals enhanced activation in a reach-selective brain area for objects located within participants’ typical hand workspaces

In recent years, there has been growing excitement within cognitive neuroscience about the concept of embodiment: How do the capabilities and limitations of our physical bodies affect neural representations in the brain? Neuropsychological and neurophysiological studies show clear evidence that short-term visuomotor experience can influence the encoding of the space around the body in parietal cortex. For example, tool-use may expand the neural representation of peripersonal space. But how is this initial spatial representation influenced by a lifetime of object-related interactions? To examine this question we used functional magnetic resonance imaging (fMRI) to investigate the neural effects of an individual's hand preferences for acting within peripersonal space. Left- and right-handed participants viewed real-world objects at different locations accessible by either the left hand, right hand, or neither hand. The superior parieto-occipital cortex (SPOC), an area most often implicated in reaching actions, showed enhanced visual responses for objects located within the range of space in which each group typically acts. Specifically, in right-handers, who strongly prefer grasping with the right hand, SPOC showed strongest activation for objects located within the range of space for the right hand only. In contrast, in left-handers, who use their two hands comparably often in visuomotor tasks, SPOC showed strongest activation for objects located within the range of space of either hand. These findings show that, even in the absence of overt responses, real 3D objects located in the individual's typical workspace for hand actions automatically invoke enhanced responses in associated visuomotor areas of the brain.

Experience-Induced Interocular Plasticity of Vision in Infancy

Animal model studies of amblyopia have generally concluded that enduring effects of monocular deprivation (MD) on visual behavior (i.e., loss of visual acuity) are limited to the deprived eye, and are restricted to juvenile life. We have previously reported, however, that lasting effects of MD on visual function can be elicited in adulthood by stimulating visuomotor experience through the non-deprived eye. To test whether stimulating experience would also induce interocular plasticity of vision in infancy, we assessed in rats from eye-opening on postnatal day (P) 15, the effect of pairing MD with the daily experience of measuring thresholds for optokinetic tracking (OKT). MD with visuomotor experience from P15 to P25 led to a ~60% enhancement of the spatial frequency threshold for OKT through the non-deprived eye during the deprivation, which was followed by loss-of-function (~60% below normal) through both eyes when the deprived eye was opened. Reduced thresholds were maintained into adulthood with binocular OKT experience from P25 to P30. The ability to generate the plasticity and maintain lost function was dependent on visual cortex. Strictly limiting the period of deprivation to infancy by opening the deprived eye at P19 resulted in a comparable loss-of-function. Animals with reduced OKT responses also had significantly reduced visual acuity, measured independently in a discrimination task. Thus, experience-dependent cortical plasticity that can lead to amblyopia is present earlier in life than previously recognized.

Short-term motor plasticity revealed in a visuomotor decision-making task

Selecting and executing an action toward only one object in our complex environments presents the visuomotor system with a significant challenge. To overcome this problem, the motor system is thought to simultaneously encode multiple motor plans, which then compete for selection. The decision between motor plans is influenced both by incoming sensory information and previous experience—which itself is comprised of long-term (e.g. weeks, months) and recent (seconds, minutes, hours) information. In this study, we were interested in how the recent trial-to-trial visuomotor experience would be factored into upcoming movement decisions made between competing potential targets. To this aim, we used a unique rapid reaching task to investigate how reach trajectories would be spatially influenced by previous decisions. Our task required subjects to initiate speeded reaches toward multiple potential targets before one was cued in-flight. A novel statistical analysis of the reach trajectories revealed that in cases of target uncertainty, subjects initiated a spatially averaged trajectory toward the midpoint of potential target locations before correcting to the selected target location. Interestingly, when the same target location was consecutively cued, reaches were biased toward that location on the next trial and this effect accumulated across trials. Beyond providing supporting evidence that potential reach locations are encoded and compete in parallel, our results strongly suggest that this motor competition is biased by recent trial history.

Development of visuomotor representations for hand movement in young children

The stability and adaptability of visuomotor representations for hand movement in young children was investigated using a visuomotor adaptation paradigm in which the real-time visual feedback of pen movement was rotated 45 degrees clockwise during exposure trials. Four, six, and eight-year-old children performed line drawings to visual targets, from a common centered position ("center-out task"), in the horizontal plane under normal (pre-, and post-exposure), and rotated (exposure) visual feedback conditions. Analysis of pre-exposure trials indicated that older children performed faster, straighter, smoother, and showed more patterned movements than the younger children. Initial direction of movement, computed at 80 ms after movement onset, showed a progressive tuning of movement direction with increasing age. On introduction of the screen cursor rotation, all age group children showed improvement in their planning (initial directional error) and execution (movement time, movement length, root mean square error, and normalized jerk) error scores from early to late-exposure trials, but the 4-year-olds were less affected than older age children by the distortion during the early exposure period. Moreover, only the oldest group of children showed significant after-effects during post-exposure trials indicating that only this age group learned the internal model of the distorted environment. The absence of after-effects for initial movement direction observed in the two younger age groups suggest that these children might have less developed (i.e. more broad) internal visuomotor representations for hand movements, and that their internal representations are sharpened (i.e. tuned) with visuomotor experience.

Vestibular adaptation exercises and recovery: Acute stage after acoustic neuroma resection

The use of exercises in the treatment of patients with vestibular deficits has become increasingly popular, and evidence exists that these exercises are beneficial in patients with chronic vestibular deficits. The question as to whether patients with acute unilateral vestibular loss would benefit from vestibular adaptation exercises is particularly compelling, however, because animal studies have demonstrated that the acute stage after unilateral vestibular loss is a critical period for recovery. Deprivation of visuomotor experience during that period can delay the onset of recovery as well as prolong the recovery period. Patients often avoid movement during the early stage because, with movement, they experience an increase in dysequilibrium and nausea. We examined the recovery of postural stability in patients during the acute stage after resection of acoustic neuroma to determine whether vestibular adaptation exercises facilitate the onset of recovery and improve the rate of recovery. The results suggest that vestibular adaptation exercises result in improved postural stability and in a diminished perception of dysequilibrium.

Vestibular adaptation exercises and recovery: Acute stage after acoustic neuroma resection

The use of exercises in the treatment of patients with vestibular deficits has become increasingly popular, and evidence exists that these exercises are beneficial in patients with chronic vestibular deficits. The question as to whether patients with acute unilateral vestibular loss would benefit from vestibular adaptation exercises is particularly compelling, however, because animal studies have demonstrated that the acute stage after unilateral vestibular loss is a critical period for recovery. Deprivation of visuomotor experience during that period can delay the onset of recovery as well as prolong the recovery period. Patients often avoid movement during the early stage because, with movement, they experience an increase in dysequilibrium and nausea. We examined the recovery of postural stability in patients during the acute stage after resection of acoustic neuroma to determine whether vestibular adaptation exercises facilitate the onset of recovery and improve the rate of recovery. The results suggest that vestibular adaptation exercises result in improved postural stability and in a diminished perception of dysequilibrium. (OTOLARYNGOL HEAD NECK SURG 1995;113:77-87.)

Selective effects of post-imprinting anaesthesia on choice-test behaviour

Day-old chicks which are submitted to a halothane anaesthesia immediately after a 10 min. exposure to a moving model are less likely than non-treated chicks to approach this model in subsequent tests given 24 and 48 hours later. They may be unable to approach any model or they may approach the other model presented in the test situation. Modulation of responses at test depends on strength of imprinting which itself depends on attractiveness of the model and amount of following displayed during the exposure session. Results of this experiment corroborate previous results showing disruptive effects of halothane anaesthesia on behaviour in imprinted chicks, effects which are stronger if chicks had a poor visuo-motor experience at exposure session. Imprinting as a gradual acquisition process is suggested by detailed analysis of results of control and treated chicks.

Recovery of forelimb placing after lateral hypothalamic lesions in the cat: parallels and contrasts with development.

Recovery of forelimb placing after lateral hypothalamic lesions in the cat is similar in several respects to the development of placing in kittens. In both recovery and development, the sequence in which sensory systems acquire control over placing is the same: vestibular--proprioceptive--tactile--visual. In addition, within each sensory modality, placing is initially sluggish, exaggerated in amplitude, and susceptible to rapid habituation. Unlike development, however, the recovery of visually guided placing does not require visuomotor experience.

Development of orientation selectivity in the primary visual cortex of normally and dark reared kittens. II. Models.

The development of orientation selectivity in the primary visual cortex is described by first-order kinetics between three functional compartments chained in a catenary mode. A first model is presented, in which two unidirectional kinetics with constant exchange coefficients, symmetrical in their effects, function in an alternating mode depending on the presence or absence of visual experience. The failure of this model to simulate the modifications induced by a delayed visual experience, when the exchange coefficients are identified to fit normal and dark rearing, supports the hypothesis that the maturation process consequent to interaction with visual environment is dependent on the date at which it is allowed to take place. A second model is then proposed, in which exchange coefficients are piecewise linear functions of time. In order to correctly predict the functional effects of restricted visual experience following prior dark rearing, it is assumed that visuomotor experience during the critical period permits the expression of a non-linear "modifiability gradient" which may have been masked up to this point by the absence of vision or eye movements.

Early and permanent effects of monocular deprivation on pattern discrimination and visuomotor behavior in cats

Visuomotor behavior and pattern discrimination were studied in a group of cats raised with one eye closed by eyelid suturing 7–10 days after birth. At the age of 8–10 months the animals were forced to use their deprived eye by reversal of eye closure (closing the normal eye and opening the deprived one). Visuomotor behavior and pattern discrimination were tested before as well as after reverse closure, to compare performances of the deprived eye with those of the non-deprived eye. In order to get optimal visuomotor experience, the animals were kept in large playrooms for at least 4 h each day. Except for normal tactile placing responses, visually triggered extension responses and uncertain jumping, 2 years after reverse closure all other tests (visually guided reaching, visual cliff behavior, obstacle avoidance, tracking, jumping, and visual blink responses) still showed impairments; the optokinetic nystagmus was asymmetric. In contrast with this partial behavioral recovery, pattern discrimination in a simple nose-push training ☐ requiring no complicated visuomotor coordination was found to be positive. Discriminations of gratings of different orientations, starting 4 weeks after reverse closure, appeared to be normal, in comparison with performance using the non-deprived eye of the same cats tested before reverse closure. Form discrimination was also found to be positive; some monocularly deprived cats required more trials than normal cats in upright vs. reversed solid triangles discrimination, but succeeding form problems were mastered within the same range as found in normal cats. Apparently behavioral defects after monocular deprivation are due to deficiencies in visuomotor control rather than in pattern identification.