Visual guidance fine-tunes probing movements of an insect appendage.

Visually guided reaching, a regular feature of human life, comprises an intricate neural control task. It includes identifying the target's position in 3D space, passing the representation to the motor system that controls the respective appendages, and adjusting ongoing movements using visual and proprioceptive feedback. Given the complexity of the neural control task, invertebrates, with their numerically constrained central nervous systems, are often considered incapable of this level of visuomotor guidance. Here, we provide mechanistic insights into visual appendage guidance in insects by studying the probing movements of the hummingbird hawkmoth's proboscis as they search for a flower's nectary. We show that visually guided proboscis movements fine-tune the coarse control provided by body movements in flight. By impairing the animals' view of their proboscis, we demonstrate that continuous visual feedback is required and actively sought out to guide this appendage. In doing so, we establish an insect model for the study of neural strategies underlying eye-appendage control in a simple nervous system.

Factors governing the assignment of visual consequence to the corresponding action.

To achieve fast feedback control of voluntary movements, the visual consequences of our motor commands need to be quickly identified and analyzed by the motor control processes in the brain. These processes work remarkably well even in complex visual environments and in the face of discrepancies between physical actuator and visually perceived effect, e.g. when moving a computer mouse on a visually crowded screen. Here, we use an ambiguous situation in which a single cursor could be controlled by either the left or the right hand to determine the visual and cognitive factors that determine the assignment of a visual stimulus to the corresponding motor command. Our results demonstrate that the visuomotor system is exquisitely sensitive to the spatio-temporal correlation between cursor and hands, learning the appropriate mapping implicitly within several minutes. In contrast, spatial proximity between end effector and visual consequence has an immediate but only transient effect on the assignment process. Finally, an explicit instruction about which hand controls the cursor only has a minor influence when the instruction is presented first. These findings provide insight into the relative importance of the factors that determine the binding of visual information to the corresponding motor structures to enable fast feedback control.NEW & NOTEWORTHY For efficient visuomotor online control, the brain needs to solve the correspondence problem between an ongoing movement and its visual consequences. Here, we challenge the visuomotor system with an ambiguous reaching task, in which the visual feedback was controlled by either hand or by a combination of both. Our findings characterize the properties of a flexible assignment process that quickly takes into account the spatio-temporal properties of movements and the visual scene.

Neuropsychology of posteromedial parietal cortex and conversion factors from Mild Cognitive Impairment to Alzheimer's disease: systematic search and state-of-the-art review.

In the present review, we discuss the rationale and the clinical implications of assessing visuospatial working memory (VSWM), awareness of memory deficits, and visuomotor control in patients with mild cognitive impairment (MCI). These three domains are related to neural activity in the posteromedial parietal cortex (PMC) whose hypoactivation seems to be a significant predictor of conversion from MCI to Alzheimer's disease (AD) as indicated by recent neuroimaging evidence. A systematic literature search was performed up to May 2021. Forty-eight studies were included: 42 studies provided analytical cross-sectional data and 6 studies longitudinal data on conversion rates. Overall, these studies showed that patients with MCI performed worse than healthy controls in tasks assessing VSWM, awareness of memory deficits, and visuomotor control; in some cases, MCI patients' performance was comparable to that of patients with overt dementia. Deficits in VSWM and metamemory appear to be significant predictors of conversion. No study explored the relationship between visuomotor control and conversion. Nevertheless, it has been speculated that the assessment of visuomotor abilities in subjects at high AD risk might be useful to discriminate patients who are likely to convert from those who are not. Being able to indirectly estimate PMC functioning through quick and easy neuropsychological tasks in outpatient settings may improve diagnostic and prognostic accuracy, and therefore, the quality of the MCI patient's management.

Gaze control during reaching is flexibly modulated to optimize task outcome.

When reaching for an object with the hand, the gaze is usually directed at the target. In a laboratory setting, fixation is strongly maintained at the reach target until the reaching is completed, a phenomenon known as "gaze anchoring." While conventional accounts of such tight eye-hand coordination have often emphasized the internal synergetic linkage between both motor systems, more recent optimal control theories regard motor coordination as the adaptive solution to task requirements. We here investigated to what degree gaze control during reaching is modulated by task demands. We adopted a gaze-anchoring paradigm in which participants had to reach for a target location. During the reach, they additionally had to make a saccadic eye movement to a salient visual cue presented at locations other than the target. We manipulated the task demands by independently changing reward contingencies for saccade reaction time (RT) and reaching accuracy. On average, both saccade RTs and reach error varied systematically with reward condition, with reach accuracy improving when the saccade was delayed. The distribution of the saccade RTs showed two types of eye movements: fast saccades with short RTs, and voluntary saccade with longer RTs. Increased reward for high reach accuracy reduced the probability of fast saccades but left their latency unchanged. The results suggest that gaze anchoring acts through a suppression of fast saccades, a mechanism that can be adaptively adjusted to the current task demands.NEW & NOTEWORTHY During visually guided reaching, our eyes usually fixate the target and saccades elsewhere are delayed ("gaze anchoring"). We here show that the degree of gaze anchoring is flexibly modulated by the reward contingencies of saccade latency and reach accuracy. Reach error became larger when saccades occurred earlier. These results suggest that early saccades are costly for reaching and the brain modulates inhibitory online coordination from the hand to the eye system depending on task requirements.

Stereopsis contributes to the predictive control of grip forces during prehension.

Binocular viewing is associated with a superior prehensile performance, which is particularly evident in the latter part of the reach as the hand approaches and makes contact with the target object. However, the visuomotor mechanisms through which binocular vision serves prehension are not fully understood. This study assessed the role of stereopsis in the predictive control of grasping by measuring grip force. Twenty participants performed a precision reach-to-grasp task in four viewing conditions: binocular, monocular, and with reduced stereoacuity (200 arc sec, > 400 arc sec). Monocular, compared to binocular viewing, was associated with a fourfold increase in grasp errors, a 56% increase in grasp duration, 22% decrease in grip force at 50 ms following grasp initiation, and the time of peak force occurred 40% later after grasp initiation (all p < 0.05). Grasp performance was also disrupted when viewing with reduced stereoacuity. Notably, grip force at the time of object lift-off was comparable between all viewing conditions. These results demonstrate that binocular stereopsis contributes to the efficient programming of grip forces. Specifically, stereopsis may provide important sensory information that enables the central nervous system to engage in predictive control of grasping.

Eye movement influences on coupled and decoupled eye-hand coordination tasks.

Visually guided reaching precision and accuracy depend on the level of coupling between movements of the eyes and hand. In the present study, participants performed central fixations and either saccadic or smooth pursuit eye movements during fast and accurate reaching tasks involving eye-hand coupling and decoupling to better understand type of eye movement influence over upper limb control. Some eye-hand coupling and decoupling tasks also included hand reversals, where the hand moves away from the target to direct a cursor toward the target to account for various levels of hand-cursor and eye-cursor coupling. Regardless of eye-movement type, eye-hand-cursor coupling produced an endpoint accuracy advantage over decoupling. Use of hand reversal decreased peak speed and increased response time of the hand, whether considering fixation or a given eye movement. Use of smooth pursuit slowed hand movements relative to saccades, yet improved endpoint accuracy. Compared to central fixations, using smooth pursuit also slowed hand movements, while using saccades decreased, thus improved, hand reaction times. Data suggest an advantage, when using smooth pursuit to track the hand movement for the greatest endpoint accuracy, an advantage when using saccades for the fastest movements, and an eye-hand coupling advantage when using saccades for the shortest reactions. Researchers should provide clear eye-movement instructions for participants and/or monitor the eyes when assessing similar upper limb control to account for possible differences in eye movements used. Moreover, the type of eye movement chosen for participants should correspond to the primary goal of the task.

Seeing motion of controlled object improves grip timing in adults with autism spectrum condition: evidence for use of inverse dynamics in motor control.

Previous studies (Haswell et al. in Nat Neurosci 12:970-972, 2009; Marko et al. in Brain J Neurol 138:784-797, 2015) reported that people with autism rely less on vision for learning to reach in a force field. This suggested a possibility that they have difficulties in extracting force information from visual motion signals, a process called inverse dynamics computation. Our recent study (Takamuku et al. in J Int Soc Autism Res 11:1062-1075, 2018) examined the ability of inverse computation with two perceptual tasks and found similar performances in typical and autistic adults. However, this tested the computation only in the context of sensory perception while it was possible that the suspected disability is specific to the motor domain. Here, in order to address the concern, we tested the use of inverse dynamics computation in the context of motor control by measuring changes in grip timing caused by seeing/not seeing a controlled object. The motion of the object was informative of its inertial force and typical participants improved their grip timing based on the visual feedback. Our interest was on whether the autism participants show the same improvement. While some autism participants showed atypical hand slowing when seeing the controlled object, we found no evidence of abnormalities in the inverse computation in our grip timing task or in a replication of the perceptual task. This suggests that the ability of inverse dynamics computation is preserved not only for sensory perception but also for motor control in adults with autism.

The relationship between the implicit visuomotor control and the motor planning accuracy.

It has been well established that an implicit motor response can be elicited by a target perturbation or a visual background motion during a reaching movement. Computational studies have suggested that the mechanism of this response is based on the error signal between the efference copy and the actual sensory feedback. If the implicit motor response is based on the efference copy, the motor command accuracy would affect the amount of the modulation of the motor response. Therefore, the purpose of the current study was to investigate the relationship between the implicit motor response and the motor planning accuracy. We used a memory-guided reaching task and a manual following response (MFR) which is induced by visual grating motion. Participants performed reaching movements toward a memorized-target location with a beep cue which was presented 0 or 3 s after the target disappeared (0-s delay and 3-s delay conditions). Leftward or rightward visual grating motion was applied 400 ms after the cue. In addition, an event-related potential (ERP) was recorded during the reaching task, which reflects the motor command accuracy. Our results showed that the N170 ERP amplitude in the parietal electrodes and the MFR amplitude were significantly larger for the 3-s delay condition than the 0-s delay condition. These results suggest that the motor planning accuracy affects the amount of the implicit visuomotor response. Furthermore, there was a significant within-subjects correlation between the MFR and the N170 amplitude, which could corroborate the relationship between the implicit motor response and the motor planning accuracy.

The influence of the Sander parallelogram illusion and early, middle and late vision on goal-directed reaching and grasping.

Vision is one of the most robust sensory inputs used for the execution of goal-directed actions. Despite a history of extensive visuomotor research, how individuals process visual context for the execution of movements continues to be debated. This experiment examines how early, middle and late visuomotor control is impacted by illusory characteristics in a reaching and grasping task. Participants either manually estimated or reached out and picked up a three-dimensional target bar resting on a two-dimensional picture of the Sander parallelogram illusion. Participants performed their grasps within a predefined time movement window based on their own average grasp time, allowing for the manipulation of visual feedback. On some trials, vision was only available before the response cue (an auditory tone), while on others vision was occluded until the response cue, becoming available for either the full, early, middle or late portions of the movement. While results showed that the effect of the illusion was stronger on manual estimations than on grasping, maximum grip apertures in the occluded vision and early vision grasping conditions were also consistent to a lesser extent with the illusion. The late vision condition showed longer movement time, wrist deceleration period, time to maximum grip aperture and lower maximum velocity. These findings indicate that visual context affects visuomotor control distinctly depending on when vision is available, and supports the notion that human vision is comprised of two functionally and anatomically distinct systems.

Looking up while reaching out: the neural correlates of making eye and arm movements in different spatial planes.

Standard visually guided reaching begins with foveation of a target of interest followed by an arm movement to the same spatial location. However, many visually guided arm movements, as well as a majority of imaging studies examining such movements, require participants to perform non-standard visuomotor mappings where the locations of gaze and arm movements are spatially dissociated (e.g. gaze fixation peripheral to the target of a reaching movement, or use of a tool such as a joystick while viewing stimuli on a screen). In this study, we compare brain activity associated with the production of standard visually guided arm movements to activity during a visuomotor mapping where saccades and reaches were made in different spatial planes. Multi-voxel pattern analysis revealed that while spatial patterns of voxel activity remain quite similar for the two visuomotor mappings during presentation of a cue for movement, patterns of activity become increasingly more discriminative throughout the brain as planning progresses toward motor execution. Decoding of the visuomotor mappings occurs throughout visuomotor-related regions of the brain including the premotor, primary motor and somatosensory, posterior parietal, middle occipital, and medial occipital cortices, and in the cerebellum. These results show that relative to standard visuomotor tasks, activity differs substantially in areas throughout the brain when a task requires an implicit sensorimotor recalibration.

Obeying the law: speed-precision tradeoffs and the adherence to Weber's law in 2D grasping.

Visually guided actions toward two-dimensional (2D) and three-dimensional (3D) objects show different patterns of adherence to Weber's law. In 3D grasping, Just Noticeable Differences (JNDs) do not scale with object size, violating Weber's law. Conversely, JNDs in 2D grasping increase with size, showing a pattern of scaler variability between aperture and JND, as predicted by Weber's law. In the current study, we tested whether such scaler variability in 2D grasping reflects genuine adherence to Weber's law. Alternatively, it could be potentially accounted for by a speed-precision tradeoff effect due to an increase in aperture velocity with size. In two experiments, we modified the relation between aperture velocity and size in 2D grasping and tested whether movement trajectories still adhere to Weber's law. In Experiment 1, we aimed to equate aperture velocities between different-sized objects by pre-adjusting the initial finger aperture to match the target's size. In Experiment 2, we reversed the relation between size and velocity by asking participants to hold their fingers wide open prior to grasp, resulting in faster velocities for smaller rather than for larger objects. The results of the two experiments showed that although aperture velocities did not increase with size, adherence to Weber's law was still maintained. These results indicate that the adherence to Weber's law during 2D grasping cannot be accounted for by a speed-precision tradeoff effect, but rather represents genuine reliance on relative, perceptually based computations in visuomotor interactions with 2D objects.

Object complexity modulates the association between action and perception in childhood.

Vision for action and vision for perception both rely on shape representations derived within the visual system. Whether the same psychological and neural mechanisms underlie both forms of behavior remains hotly contested, and whether this arrangement is equivalent in adults and children is controversial as well. To address these outstanding questions, we used an established psychophysical heuristic, Weber's law, which, in adults, has typically been observed for perceptual judgment tasks but not for actions such as grasping. We examined whether this perception-action dissociation in Weber's law was present in childhood as it is in adulthood and whether it was modulated by stimulus complexity. Two major results emerged. First, although adults evinced visuomotor behavior that violated Weber's law, young children (4.5-6.5 years) adhered to Weber's law when they grasped complex objects ("Efron" blocks), which varied along both the graspable and non-graspable dimensions to maintain a constant surface area, but not when they grasped simple objects, which varied only along the graspable dimension. Second, adherence to Weber's law was found across all ages in the context of a perceptual task. Together, these findings suggest that, in early childhood, visuomotor representations are modulated by perceptual representations, particularly when a refined description of object shape is needed.

Two subdivisions of macaque LIP process visual-oculomotor information differently.

Although the cerebral cortex is thought to be composed of functionally distinct areas, the actual parcellation of area and assignment of function are still highly controversial. An example is the much-studied lateral intraparietal cortex (LIP). Despite the general agreement that LIP plays an important role in visual-oculomotor transformation, it remains unclear whether the area is primary sensory- or motor-related (the attention-intention debate). Although LIP has been considered as a functionally unitary area, its dorsal (LIPd) and ventral (LIPv) parts differ in local morphology and long-distance connectivity. In particular, LIPv has much stronger connections with two oculomotor centers, the frontal eye field and the deep layers of the superior colliculus, than does LIPd. Such anatomical distinctions imply that compared with LIPd, LIPv might be more involved in oculomotor processing. We tested this hypothesis physiologically with a memory saccade task and a gap saccade task. We found that LIP neurons with persistent memory activities in memory saccade are primarily provoked either by visual stimulation (vision-related) or by both visual and saccadic events (vision-saccade-related) in gap saccade. The distribution changes from predominantly vision-related to predominantly vision-saccade-related as the recording depth increases along the dorsal-ventral dimension. Consistently, the simultaneously recorded local field potential also changes from visual evoked to saccade evoked. Finally, local injection of muscimol (GABA agonist) in LIPv, but not in LIPd, dramatically decreases the proportion of express saccades. With these results, we conclude that LIPd and LIPv are more involved in visual and visual-saccadic processing, respectively.

Vision for Prehension in the Medial Parietal Cortex.

In the last 2 decades, the medial posterior parietal area V6A has been extensively studied in awake macaque monkeys for visual and somatosensory properties and for its involvement in encoding of spatial parameters for reaching, including arm movement direction and amplitude. This area also contains populations of neurons sensitive to grasping movements, such as wrist orientation and grip formation. Recent work has shown that V6A neurons also encode the shape of graspable objects and their affordance. In other words, V6A seems to encode object visual properties specifically for the purpose of action, in a dynamic sequence of visuomotor transformations that evolve in the course of reach-to-grasp action.We propose a model of cortical circuitry controlling reach-to-grasp actions, in which V6A acts as a comparator that monitors differences between current and desired hand positions and configurations. This error signal could be used to continuously update the motor output, and to correct reach direction, hand orientation, and/or grip aperture as required during the act of prehension.In contrast to the generally accepted view that the dorsomedial component of the dorsal visual stream encodes reaching, but not grasping, the functional properties of V6A neurons strongly suggest the view that this area is involved in encoding all phases of prehension, including grasping.

Neural correlates of visuomotor adjustments during scaling of human finger movements.

Visually guided finger movements include online feedback of current effector position to guide target approach. This visual feedback may be scaled or otherwise distorted by unpredictable perturbations. Although adjustments to visual feedback scaling have been studied before, the underlying brain activation differences between upscaling (visual feedback larger than real movement) and downscaling (feedback smaller than real movement) are currently unknown. Brain activation differences between upscaling and downscaling might be expected because within-trial adjustments during upscaling require corrective backwards accelerations, whereas correcting for downscaling requires forward accelerations. In this behavioural and fMRI study we investigated adjustments during up- and downscaling in a target-directed finger flexion-extension task with real-time visual feedback. We found that subjects made longer and more complete within-trial corrections for downscaling perturbations than for upscaling perturbations. The finger task activated primary motor (M1) and somatosensory (S1) areas, premotor and parietal regions, basal ganglia, and cerebellum. General scaling effects were seen in the right pre-supplementary motor area, dorsal anterior cingulate cortex, inferior parietal lobule, and dorsolateral prefrontal cortex. Stronger activations for down- than for upscaling were observed in M1, supplementary motor area (SMA), S1 and anterior cingulate cortex. We argue that these activation differences may reflect differing online correction for upscaling vs. downscaling during finger flexion-extension.

Visuomotor signals for reaching movements in the rostro-dorsal sector of the monkey thalamic reticular nucleus.

The thalamic reticular nucleus (TRN) collects inputs from the cerebral cortex and thalamus and, in turn, sends inhibitory outputs to the thalamic relay nuclei. This unique connectivity suggests that the TRN plays a pivotal role in regulating information flow through the thalamus. Here, we analyzed the roles of TRN neurons in visually guided reaching movements. We first used retrograde transneuronal labeling with rabies virus, and showed that the rostro-dorsal sector of the TRN (TRNrd) projected disynaptically to the ventral premotor cortex (PMv). In other experiments, we recorded neurons from the TRNrd or PMv while monkeys performed a visuomotor task. We found that neurons in the TRNrd and PMv showed visual-, set-, and movement-related activity modulation. These results indicate that the TRNrd, as well as the PMv, is involved in the reception of visual signals and in the preparation and execution of reaching movements. The fraction of neurons that were non-selective for the location of visual signals or the direction of reaching movements was greater in the TRNrd than in the PMv. Furthermore, the fraction of neurons whose activity increased from the baseline was greater in the TRNrd than in the PMv. The timing of activity modulation of visual-related and movement-related neurons was similar in TRNrd and PMv neurons. Overall, our data suggest that TRNrd neurons provide motor thalamic nuclei with inhibitory inputs that are predominantly devoid of spatial selectivity, and that these signals modulate how these nuclei engage in both sensory processing and motor output during visually guided reaching behavior.

Prism adaptation speeds reach initiation in the direction of the prism after-effect.

Damage to the temporal-parietal cortex in the right hemisphere often leads to spatial neglect-a disorder in which patients are unable to attend to sensory input from their contralesional (left) side. Neglect has been associated with both attentional and premotor deficits. That is, in addition to having difficulty with attending to the left side, patients are often slower to initiate leftward vs. rightward movements (i.e., directional hypokinesia). Previous research has indicated that a brief period of adaptation to rightward shifting prisms can reduce symptoms of neglect by adjusting the patient's movements leftward, toward the neglected field. Although prism adaptation has been shown to reduce spatial attention deficits in patients with neglect, very little work has examined the effects of prisms on premotor symptoms. In the current study, we examined this in healthy individuals using leftward shifting prisms to induce a rightward shift in the egocentric reference frame, similar to neglect patients prior to prism adaptation. Specifically, we examined the speed with which healthy participants initiated leftward and rightward reaches (without visual feedback) prior to and following adaptation to either 17° leftward (n = 16) or 17° rightward (n = 15) shifting prisms. Our results indicated that, following adaptation, participants were significantly faster to initiate reaches towards targets located in the direction opposite the prism shift. That is, participants were faster to initiate reaches to right targets following leftward prism adaptation and were faster to initiate reaches to left targets following rightward prism adaptation. Overall, these results are consistent with the idea that prism adaptation can influence the speed with which a reach can be initiated toward a target in the direction opposite the prism shift, possibly through altering activity in neural circuits involved in reach planning.

Grasping occluded targets: investigating the influence of target visibility, allocentric cue presence, and direction of motion on gaze and grasp accuracy.

Participants executed right-handed reach-to-grasp movements toward horizontally translating targets. Visual feedback of the target when reaching, as well as the presence of additional cues placed above and below the target's path, was manipulated. Comparison of average fixations at reach onset and at the time of the grasp suggested that participants accurately extrapolated the occluded target's motion prior to reach onset, but not after the reach had been initiated, resulting in inaccurate grasp placements. Final gaze and grasp positions were more accurate when reaching for leftward moving targets, suggesting individuals use different grasp strategies when reaching for targets traveling away from the reaching hand. Additional cue presence appeared to impair participants' ability to extrapolate the disappeared target's motion, and caused grasps for occluded targets to be less accurate. Novel information is provided about the eye-hand strategies used when reaching for moving targets in unpredictable visual conditions.

Rapid Visuomotor Corrective Responses during Transport of Hand-Held Objects Incorporate Novel Object Dynamics.

Numerous studies have shown that people are adept at learning novel object dynamics, linking applied force and motion, when performing reaching movements with hand-held objects. Here we investigated whether the control of rapid corrective arm responses, elicited in response to visual perturbations, has access to such newly acquired knowledge of object dynamics. Participants first learned to make reaching movements while grasping an object subjected to complex load forces that depended on the distance and angle of the hand from the start position. During a subsequent test phase, we examined grip and load force coordination during corrective arm movements elicited (within ∼150 ms) in response to viewed sudden lateral shifts (1.5 cm) in target or object position. We hypothesized that, if knowledge of object dynamics is incorporated in the control of the corrective responses, grip force changes would anticipate the unusual load force changes associated with the corrective arm movements so as to support grasp stability. Indeed, we found that the participants generated grip force adjustments tightly coupled, both spatially and temporally, to the load force changes associated with the arm movement corrections. We submit that recently learned novel object dynamics are effectively integrated into sensorimotor control policies that support rapid visually driven arm corrective actions during transport of hand held objects. Significance statement: Previous studies have demonstrated that the motor system can learn, and make use of, internal models of object dynamics to generate feedforward motor commands. However, it is not known whether such internal models are incorporated into rapid, automatic arm movement corrections that compensate for errors that arise during movement. Here we demonstrate, for the first time, that internal models of novel object dynamics are integrated into rapid corrective arm movements made in response to visuomotor perturbations that, importantly, do not directly perturb the object.

Playing Action Video Games Improves Visuomotor Control.

Can playing action video games improve visuomotor control? If so, can these games be used in training people to perform daily visuomotor-control tasks, such as driving? We found that action gamers have better lane-keeping and visuomotor-control skills than do non-action gamers. We then trained non-action gamers with action or nonaction video games. After they played a driving or first-person-shooter video game for 5 or 10 hr, their visuomotor control improved significantly. In contrast, non-action gamers showed no such improvement after they played a nonaction video game. Our model-driven analysis revealed that although different action video games have different effects on the sensorimotor system underlying visuomotor control, action gaming in general improves the responsiveness of the sensorimotor system to input error signals. The findings support a causal link between action gaming (for as little as 5 hr) and enhancement in visuomotor control, and suggest that action video games can be beneficial training tools for driving.