Robert L. Whitwell

Practice makes perfect, but only with the right hand: Sensitivity to perceptual illusions with awkward grasps decreases with practice in the right but not the left hand

It has been proposed that the visual mechanisms that control well-calibrated actions, such as picking up a small object with a precision grip, are neurally distinct from those that mediate our perception of the object. Thus, grip aperture in such situations has been shown to be remarkably insensitive to many size-contrast illusions. But most of us have practiced such movements hundreds, if not thousands of times. What about less familiar and unpracticed movements? Perhaps they would be less likely to be controlled by specialized visuomotor mechanisms and would therefore be more sensitive to size-contrast illusions. To test this idea, we asked right-handed subjects to pick up small objects using either a normal precision grasp (thumb and index finger) or an awkward grasp (thumb and ring finger), in the context of the Ponzo illusion. Even though this size-contrast illusion had no effect on the scaling of the precision grasp, it did have a significant effect on the scaling of the awkward grasp. Nevertheless, after three consecutive days of practice, even the awkward grasp became resistant to the illusion. In a follow-up experiment, we found that awkward grasps with the left hand (in right handers) did not benefit from practice and remained sensitive to the illusion. We conclude that the skilled target-directed movements are controlled by visual mechanisms that are quite distinct from those controlling unskilled movements, and that these specialized visuomotor mechanisms may be lateralized to the left hemisphere.

Left handedness does not extend to visually guided precision grasping

In the present study, we measured spontaneous hand preference in a “natural” grasping task. We asked right- and left-handed subjects to put a puzzle together or to create different LEGO© models, as quickly and as accurately as possible, without any instruction about which hand to use. Their hand movements were videotaped and hand preference for grasping in ipsilateral and contralateral space was measured. Right handers showed a marked preference for their dominant hand when picking up objects; left handers, however, did not show this preference and instead used their right hand 50% of the time. Furthermore, compared to right handers, left handers used their non-dominant hand significantly more often to pick up objects in ipsilateral as well as contralateral space. Our results show that handedness in left handers does not extend to precision grasp and suggest that right handedness for visuomotor control may reflect a universal left-hemisphere specialization for this class of behaviour.

Grasping future events: explicit knowledge of the availability of visual feedback fails to reliably influence prehension

We examined whether or not conscious knowledge about the availability of visual feedback on an upcoming trial would influence the programming of a precision grip. Twenty healthy volunteers were asked to reach out and grasp objects under two viewing conditions: full visual feedback (closed loop) or no visual feedback (open loop). The two viewing conditions were presented in blocked, randomized, and alternating trial orders. Before each block of trials, participants were explicitly informed of the nature of the upcoming order of viewing conditions. Even though participants continued to scale their grip to the size of the goal objects which varied in size and distance, they opened their hand significantly wider when visual feedback was not available during movement execution. This difference was evident before peak grip aperture was reached, continued into the grip aperture closing phase, and presumably reflects the visuomotor system’s ability to build in a margin of error to compensate for the absence of visual feedback. The difference in grip aperture between closed- and open-loop trials increased as a function of distance, which suggests that the visuomotor system can make use of visual feedback given enough time, even when that feedback is not anticipated. The difference in grip aperture between closed- and open-loop trials was larger when the two visual feedback conditions were blocked than when they were either randomized or alternated. Importantly, performance did not differ between the randomized and the alternating trial blocks. In other words, despite knowledge of the availability of visual feedback on an upcoming trial in the predictable alternating block, participants behaved no differently than they did on randomized trials. Taken together, these results suggest that motor planning tends to optimize performance largely on the basis of what has happened regularly in the past and cannot take full advantage of conscious knowledge of what will happen on a future occasion.

Updating the programming of a precision grip is a function of recent history of available feedback

In a recent study (Whitwell et al. in Exp Brain Res 185:111–119, 2008), we showed that the visuomotor system is “cognitively impenetrable” to the extent that explicit predictive knowledge of the availability of visual feedback on an upcoming trial fails to optimize grasping. The results suggested that the effects of trial history, rather than the anticipatory knowledge of the nature of an upcoming trial, plays the most significant role in how the availability of visual feedback is exploited by the visuomotor system when programming grip aperture (e.g., opening the hand wider when visual feedback is unavailable). Here, we provide direct evidence that trial history indeed plays a critical role in the programming of grip aperture. Twelve individuals grasped objects of three different sizes placed at one of two distances either with or without visual feedback of the hand and object (closed- or open-loop trials, respectively). Runs of four consecutive closed- or open-loop trials were interleaved with sequences of closed and open-loop trials that alternated back and forth from trial to trial. Peak grip aperture (PGA) decreased linearly with successive closed-loop trials and increased linearly with successive open-loop trials. We also compared PGA for trials that were preceded by a run of four consecutive closed- (or open-loop) trials with trials that were preceded by only one closed- (or open-loop) trial. This analysis indicated that consistency in the runs of closed- or open-loop trials significantly reduced the effect of the availability of feedback on grasping in the trial following the run. We conclude that while the margin of error observed in precision grasping is largely a function of the availability of visual feedback on the current trial, it is evidently also a function of the recent history of the availability of visual feedback on previous trials.

The Two Visual Systems Hypothesis: New Challenges and Insights from Visual form Agnosic Patient DF

Patient DF, who developed visual form agnosia following carbon monoxide poisoning, is still able to use vision to adjust the configuration of her grasping hand to the geometry of a goal object. This striking dissociation between perception and action in DF provided a key piece of evidence for the formulation of Goodale and Milner’s Two Visual Systems Hypothesis (TVSH). According to the TVSH, the ventral stream plays a critical role in constructing our visual percepts, whereas the dorsal stream mediates the visual control of action, such as visually guided grasping. In this review, we discuss recent studies of DF that provide new insights into the functional organization of the dorsal and ventral streams. We confirm recent evidence that DF has dorsal as well as ventral brain damage – and that her dorsal-stream lesions and surrounding atrophy have increased in size since her first published brain scan. We argue that the damage to DF’s dorsal stream explains her deficits in directing actions at targets in the periphery. We then focus on DF’s ability to accurately adjust her in-flight hand aperture to changes in the width of goal objects (grip scaling) whose dimensions she cannot explicitly report. An examination of several studies of DF’s grip scaling under natural conditions reveals a modest though significant deficit. Importantly, however, she continues to show a robust dissociation between form vision for perception and form vision-for-action. We also review recent studies that explore the role of online visual feedback and terminal haptic feedback in the programming and control of her grasping. These studies make it clear that DF is no more reliant on visual or haptic feedback than are neurologically intact individuals. In short, we argue that her ability to grasp objects depends on visual feedforward processing carried out by visuomotor networks in her dorsal stream that function in the much the same way as they do in neurologically intact individuals.

Real-time vision, tactile cues, and visual form agnosia: removing haptic feedback from a “natural” grasping task induces pantomime-like grasps

Investigators study the kinematics of grasping movements (prehension) under a variety of conditions to probe visuomotor function in normal and brain-damaged individuals. “Natural” prehensile acts are directed at the goal object and are executed using real-time vision. Typically, they also entail the use of tactile, proprioceptive, and kinesthetic sources of haptic feedback about the object (“haptics-based object information”) once contact with the object has been made. Natural and simulated (pantomimed) forms of prehension are thought to recruit different cortical structures: patient DF, who has visual form agnosia following bilateral damage to her temporal-occipital cortex, loses her ability to scale her grasp aperture to the size of targets (“grip scaling”) when her prehensile movements are based on a memory of a target previewed 2 s before the cue to respond or when her grasps are directed towards a visible virtual target but she is denied haptics-based information about the target. In the first of two experiments, we show that when DF performs real-time pantomimed grasps towards a 7.5 cm displaced imagined copy of a visible object such that her fingers make contact with the surface of the table, her grip scaling is in fact quite normal. This finding suggests that real-time vision and terminal tactile feedback are sufficient to preserve DF’s grip scaling slopes. In the second experiment, we examined an “unnatural” grasping task variant in which a tangible target (along with any proxy such as the surface of the table) is denied (i.e., no terminal tactile feedback). To do this, we used a mirror-apparatus to present virtual targets with and without a spatially coincident copy for the participants to grasp. We compared the grasp kinematics from trials with and without terminal tactile feedback to a real-time-pantomimed grasping task (one without tactile feedback) in which participants visualized a copy of the visible target as instructed in our laboratory in the past. Compared to natural grasps, removing tactile feedback increased RT, slowed the velocity of the reach, reduced in-flight grip aperture, increased the slopes relating grip aperture to target width, and reduced the final grip aperture (FGA). All of these effects were also observed in the real time-pantomime grasping task. These effects seem to be independent of those that arise from using the mirror in general as we also compared grasps directed towards virtual targets to those directed at real ones viewed directly through a pane of glass. These comparisons showed that the grasps directed at virtual targets increased grip aperture, slowed the velocity of the reach, and reduced the slopes relating grip aperture to the widths of the target. Thus, using the mirror has real consequences on grasp kinematics, reflecting the importance of task-relevant sources of online visual information for the programming and updating of natural prehensile movements. Taken together, these results provide compelling support for the view that removing terminal tactile feedback, even when the grasps are target-directed, induces a switch from real-time visual control towards one that depends more on visual perception and cognitive supervision. Providing terminal tactile feedback and real-time visual information can evidently keep the dorsal visuomotor system operating normally for prehensile acts.

Explicit knowledge about the availability of visual feedback affects grasping with the left but not the right hand.

Previous research (Whitwell et al. in Exp Brain Res 188:603–611, 2008; Whitwell and Goodale in Exp Brain Res 194:619–629, 2009) has shown that trial history, but not anticipatory knowledge about the presence or absence of visual feedback on an upcoming trial, plays a vital role in determining how that feedback is exploited when grasping with the right hand. Nothing is known about how the non-dominant left hand behaves under the same feedback regimens. In present study, therefore, we compared peak grip aperture (PGA) for left- and right-hand grasps executed with and without visual feedback (i.e., closed- vs. open-loop conditions) in right-handed individuals under three different trial schedules: the feedback conditions were blocked separately, they were randomly interleaved, or they were alternated. When feedback conditions were blocked, the PGA was much larger for open-loop trials as compared to closed-loop trials, although this difference was more pronounced for right-hand grasps than left-hand grasps. Like Whitwell et al., we found that mixing open- and closed-loop trials together, compared to blocking them separately, homogenized the PGA for open- and closed-loop grasping in the right hand (i.e., the PGAs became smaller on open-loop trials and larger on closed-loop trials). In addition, the PGAs for right-hand grasps were entirely determined by trial history and not by knowledge of whether or not visual feedback would be available on an upcoming trial. In contrast to grasps made with the right hand, grasps made by the left hand were affected both by trial history and by anticipatory knowledge of the upcoming visual feedback condition. But these effects were observed only on closed-loop trials, i.e., the PGAs of grasps made with the left hand on closed-loop trials were smaller when participants could anticipate the availability of feedback on an upcoming trial (alternating trials) than when they could not (randomized trials). In contrast, grasps made with the left hand on open-loop trials exhibited the same large PGAs under all feedback schedules: blocked, random, or alternating. In other words, there was no evidence for homogenization. Taken together, these results suggest that in addition to the real-time demands of the task, such as the target’s size and position and the availability of visual feedback, the initial (i.e., pre-movement) programming of right-hand grasping relies on what happened on the previous trial, whereas the programming of left-hand grasping is more cognitively supervised and exploits explicit information about trial order to prepare for an upcoming trial.

Patient DF’s visual brain in action: Visual feedforward control in visual form agnosia

Patient DF, who developed visual form agnosia following ventral-stream damage, is unable to discriminate the width of objects, performing at chance, for example, when asked to open her thumb and forefinger a matching amount. Remarkably, however, DF adjusts her hand aperture to accommodate the width of objects when reaching out to pick them up (grip scaling). While this spared ability to grasp objects is presumed to be mediated by visuomotor modules in her relatively intact dorsal stream, it is possible that it may rely abnormally on online visual or haptic feedback. We report here that DFs grip scaling remained intact when her vision was completely suppressed during grasp movements, and it still dissociated sharply from her poor perceptual estimates of target size. We then tested whether providing trial-by-trial haptic feedback after making such perceptual estimates might improve DFs performance, but found that they remained significantly impaired. In a final experiment, we re-examined whether DFs grip scaling depends on receiving veridical haptic feedback during grasping. In one condition, the haptic feedback was identical to the visual targets. In a second condition, the haptic feedback was of a constant intermediate width while the visual target varied trial by trial. Despite this incongruent feedback, DF still scaled her grip aperture to the visual widths of the target blocks, showing only normal adaptation to the false haptically-experienced width. Taken together, these results strengthen the view that DFs spared grasping relies on a normal mode of dorsal-stream functioning, based chiefly on visual feedforward processing.

Grasping without vision: time normalizing grip aperture profiles yields spurious grip scaling to target size.

The analysis of normalized movement trajectories is a popular and informative technique used in investigations of visuomotor control during goal-directed acts like reaching and grasping. This technique typically involves standardizing measures against the amplitude of some other variable - most typically time. Here, we show that this normalizing technique can lead to some surprising results. In the first of two experiments, we asked participants to grasp target objects without ever seeing them from trial to trial. In the second experiment, participants were given a brief preview of the target and were then cued 3s later to pick it up while vision was prevented. Critically, on some trials during the delay period and unbeknownst to the participants, the previewed target was swapped for a new unseen one. The results of both experiments show that time-normalized measures of grip aperture during the closing phase of the movement appear to be scaled to target size well before the fingers make contact with the target - even though participants had no idea what the size of the target was that they were grasping. In contrast, a classical measure of anticipatory grip scaling, maximum grip aperture, did not show scaling to target size. As we demonstrate, however, in both experiments, movement time was longer for the larger target than the smaller ones. Thus, the comparisons of time-normalized grip aperture, particularly during the closing phase of the movements, were made across different points in real time. Taken together, the results of these experiments highlight a need for caution when investigators interpret differences in time-normalized dependent measures - particularly when the effect of interest is correlated with the dependent measure and a third variable (e.g., movement time) that is used to standardize the dependent measure.

Real and illusory issues in the illusion debate (Why two things are sometimes better than one): Commentary on Kopiske et al. (2016)

Nearly twenty-five years ago, Goodale and Milner (1992) proposed that the visual networks that generate our perception of the world are anatomically and functionally distinct from those that mediate the visual control of action. Some of the most intriguing, but controversial, evidence for dissociations between vision-for-perception and vision-foraction has come from studies of visual illusions of size, in which the context (surrounding objects, features, or pictorial cues) makes a target object appear to be bigger or smaller than it really is (for review, see Goodale & Ganel, 2016). The first study to demonstrate a dissociation between perceptual report and grasping in the context of sizecontrast illusions was carried out by Aglioti, DeSouza, and Goodale (1995) who showed that the scaling of grip aperture in-flight was less sensitive than judgements of disk size to the Ebbinghaus illusion. Not long after, Haffenden and Goodale (1998) reported a similar finding: grip aperture inflight escaped the influence of the illusion, whereas the illusion affected performance in a manual size-matching task in which participants were asked to open their index finger and thumb to indicate the perceived size of a disk. This measure e a kind perceptual report or judgement e is akin to the typical magnitude estimation paradigms used in conventional psychophysics, but with the virtue that it makes use of the same effector that is used in the grasping task. In the case of the Ebbinghaus illusion, it has been argued that the small effect that the illusion appears to have on grip aperture reflects an intrusion of explicit cognitive supervision in the control of the grasping movement (Gonzalez, Ganel, & Goodale, 2006), particularly early on in task performance (Gonzalez, Ganel, Whitwell, Morrissey, & Goodale, 2008). It has also been argued that the influence of the display is a reflection of the visuomotor systems attempt to avoid having the fingers collide with the apparent obstacles created by elements in the contextual display (Haffenden, Schiff, & Goodale, 2001). Importantly, because the obstacle avoidance strategy and the putative effect of the illusion display on grip aperture could go in the same direction, it is possible to conclude erroneously that grasps and perceptual judgements rely on the same underlying visual computations.