Edited by: Ferdinand Binkofski, RWTH Aachen University, Germany
Reviewed by: Annalisa Setti, University College Cork, Ireland; Marc Himmelbach, University Hospital Tuebingen, Germany
*Correspondence: Carys Evans
This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution and reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
Patients with apraxia perform poorly when demonstrating how an object is used, particularly when pantomiming the action. However, these patients are able to accurately identify, and to pick up and move objects, demonstrating intact ventral and dorsal stream visuomotor processing. Appropriate object manipulation for skilled use is thought to rely on integration of known and visible object properties associated with “ventro-dorsal” stream neural processes. In apraxia, it has been suggested that stored object knowledge from the ventral stream may be less readily available to incorporate into the action plan, leading to an over-reliance on the objects’ visual affordances in object-directed motor behavior. The current study examined grasping performance in left hemisphere stroke patients with (
Apraxia is a high-level movement disorder that commonly occurs after lesions to the left frontoparietal motor network. In addition to impaired gesture imitation, apraxia is recognized by performance errors when demonstrating how objects are used (Goldenberg,
Close examination of object knowledge in apraxic patients confirms that performance errors cannot be attributed to impaired ventral (vision-for-perception) or dorsal (vision-for-action) streams of the visual pathways model (Goodale and Milner,
Unlike the dorsal pathway that extends bilaterally from occipital to superior parietal and dorsal pre-motor areas, the ventro-dorsal sub-stream is left lateralized, projecting medially from occipital to left inferior parietal lobe (IPL) and ventral pre-motor regions. Through a mutual connection with the ventral stream via the left IPL, perceptual information can be incorporated into action plans (Rizzolatti and Matelli,
That said, apraxic patients have shown equivalent performance to controls when making memory-driven reach and grasp movements also reliant on the integration of ventral and dorsal processes (Ietswaart et al.,
While the research outlined suggests apraxic patients have difficulties accessing and incorporating stored knowledge of actions related to skilled use of familiar objects, it remains unclear how these patients learn to manipulate new objects. Of the few studies that have assessed this issue, Barde et al. (
The current study explored the impact of affordance on object manipulation by requiring participants to repeatedly lift and balance novel objects of differing weight distribution. Over two conditions, the weight distribution of different cylindrical objects was indicated using different object-weight associations, either by a symbolic memory-association between the color of the object and its weight distribution or by a visual-spatial cue of a “dot” over the weighted end of the object. Change in object manipulation over repeated lifts determined whether apraxic patients successfully used object knowledge obtained through experience to inform their grasp, or whether they continually relied on the visual cues to guide action.
Specifically, this study examined participants’ point of grasp along the object depending on weight distribution. When grasping unbalanced objects, healthy adults intuitively choose a grasp close to the center of mass in order to minimize the energy required by grip force to compensate for load torque (Salimi et al.,
During the memory-associated condition, when each object’s weight distribution was indicated symbolically by the color of the object, apraxic patients were expected to be impaired. Due to the symmetrical shape of the object, apraxic patients were expected to be biased towards more central grasp points and require a greater number of trials to accurately balance the object. In the visual-spatial cue condition, when the center of mass is indicated by a “dot” over the weighted end, apraxic patients may benefit from this meaningful visible cue over time to prompt a more accurate grasp-point over each trial. An alternative prediction was that apraxic patients might continue to use low-level affordance cues of object structure to indicate weight distribution, resulting in more central grasps rather than to the left or right of the object. Inappropriate manipulation of memory-associated and visual-spatial cued objects would confirm that apraxics over-rely on visual information processed by the dorsal visual stream due to ventral, stored knowledge, being unsuccessfully incorporated into the action plan via the ventro-dorsal sub-stream. Such behavior would add insight into what information apraxic patients can effectively utilize during goal directed action.
Twenty-seven right-handed participants were recruited, 13 of which had suffered a stroke (
On the basis of CT, MRI scans and clinical notes, patients who had a brain hemeorrhage or an infarct involving the left hemisphere were recruited from rehabilitation centers and National Health Hospitals within the North East of England. Patients presented with degrees of aphasia, right-sided weakness, or sensory loss. Table
Brodmann areas damaged (% = amount lesioned) | |||||
---|---|---|---|---|---|
Patient | Includes IPL | Lesion—left hemisphere lesion information on basis of acute CT/MRI report | >75% | 25–75% | <25% |
AH | N | L MCA infarct involving L putamen, internal capsule, and caudate head. Extending into L frontal white matter. | 34 | 10, 11, 25, 32, 47, 45, 46 | |
GW | Y | L temporo-parietal, basal ganglia, and parieto-occipital infarcts. | 22, 31, 37, |
6, 19, 20, 34, 36, 38 | |
JA | N | L MCA infarct. | 34, 38 | 47 | 6, 11, 20, 21, 22, 41, 44 |
SG | N | L corona radiata infarct. | |||
TY | N | L frontal MCA infarct. | 47 | 11, 38 | |
DF | - | L fronto-temporo-parietal infarct and L insula. | |||
WM | - | L total anterior circulation infarct. | |||
MB | N | L frontal lobe, thalamus, lentiform, R caudate head, bilateral basal ganglia lacunar infarcts. | |||
TM | N | Ischemeic change in the L MCA occlusion. | 42 | ||
DJ | N | L frontal MCA infarct. | 44 | 6, 38, 43 | 9 |
JS | N | Mild white matter ischemeic change. | |||
BH | N | L thalamus bleed. |
The presence of apraxia was classified on the basis of abnormal performance in one or more of the apraxia screening tools assessing gesture imitation and familiar object-use (pantomime and actual use). Further test batteries and clinical notes were used to exclude any patient presenting with global cognitive deficits or known dementia, severe receptive aphasia or failure to follow one-stage commands (according to the language comprehension token test by De Renzi and Faglioni,
Patient | Sex | Age at test (years) | Days post stroke at test | Right sided motor weakness admission | Aphasia noted on admission | Neglect/hemianopia | Language comprehension (stage reached of Token Test) |
---|---|---|---|---|---|---|---|
AH | F | 72 | 226 | Y | Y | R neglect | 6 |
GW | M | 49 | 87 | Y | Y | n.t. | 3 |
JA | F | 48 | 486 | Y | Y | N | 2 |
SG | F | 66 | 833 | Y | Y | N | 6 |
TY | M | 76 | 783 | N | Y | N | 5 |
DF | M | 70 | 754 | Y | Y | N | 6 |
WM | M | 78 | 152 | Y | N | N | 6 |
MB | F | 49 | 142 | Y | Y | N | 6 |
TM | M | 61 | 169 | Y | Y | N | 6 |
DJ | M | 84 | 130 | N | Y | N | 5 |
JS | F | 91 | 823 | Y | N | N | 6 |
BH | M | 58 | 843 | Y | N | N | 6 |
Apraxia screening | ||||||||
---|---|---|---|---|---|---|---|---|
Gesture imitation (total score) | Object use (total score) | |||||||
Patient | Hand (20) | Fingers (20) | Pantomime (53) | Actual (18) | ||||
AH | 19 | 19 | 37 | 18 | ||||
GW | 16 | 4 | 10 | 16 | ||||
JA | 19 | 20 | 36 | 16 | ||||
SG | 20 | 20 | 53 | 18 | ||||
TY | 18 | 18 | 48 | 18 | ||||
DF | 18 | 20 | 50 | 18 | ||||
WM | 20 | 20 | 48 | 18 | ||||
MB | 19 | 19 | 53 | 18 | ||||
TM | 20 | 20 | 53 | 18 | ||||
DJ | 18 | 19 | 53 | 18 | ||||
JS | 20 | 20 | 53 | 18 | ||||
BH | 20 | 20 | 51 | 18 |
Healthy age-matched control participants did not have a history of brain damage or stroke. These participants were recruited from the Psychology Department’s participant database and were given monetary compensation for their time.
The experimenter demonstrated different hand postures relative to the head and finger postures irrespective of the hands position in relation to the body. Gestures were performed “like a mirror”; the experimenter sat opposite the patient, performing each posture with their right hand to be imitated by the patients’ left hand after the demonstration had ended. Successful imitation of each gesture on the first trial was awarded two points; one point was given if the patient was successful after a further demonstration; zero points if the gesture was not imitated correctly. A total score of 20 could be achieved by imitating 10 gestures of each kind.
Participants were required to demonstrate the use of 19 objects. The experimenter presented a drawn image of each object (taken from Cycowicz et al.,
Participants were given the same verbal description of the action to be demonstrated as in the pantomime task. Eighteen of the pantomimed objects were presented; one point was given if used correctly and zero if incorrect. The incorrect use of two or more objects was considered pathological.
Five cardboard cylinder tubes (length: 24.5 cm, diameter: 3.7 cm) were used, each containing a 17 g weight (length: 2 cm, diameter: 1.5 cm) in one or both ends. The five cylindrical objects comprised of two experimental conditions: “memory-associated” and “visual-spatial cue”, and one screening condition: “neutral-control”. The “memory-associated” condition consisted of one green and one blue cylinder; when presented to the participant, the green object was weighted on the left, whereas the blue object was weighted on the right. Participants were required to remember the color-weight associations when lifting the object without a visual cue indicating weight distribution on either end of the cylinder. The visual-spatial cue condition consisted of two gray objects that were unevenly weighted, containing a weight in either the left or right end of the object. The heavier end of each object was marked with a red “dot” (1 cm diameter), which acted as a visual cue of the weight distribution when acting upon the object. Finally, the neutral-control condition consisted of one gray object that was evenly weighted with one weight in each end of the cylinder. This screened for any confounds such as visuospatial neglect or comprehension issues that would impact task performance. In addition to the main objects, two white practice cylinders were used when giving task instructions: one evenly-weighted (length: 42 cm, diameter: 1.5 cm) and one unevenly-weighted object (length: 46, diameter 1.7 cm, 34 g weight on the right side). The practice cylinders did not resemble test objects in size and weight to minimize priming effects of grasping these objects prior to the main experiment.
A horizontal bar (length: 30 cm, diameter: 0.5 cm) was positioned perpendicular to the participant, 35 cm in front of the participant and 24 cm above the table. Both the experimenter and participant used the bar to indicate the extent to which the object was balanced. For the duration of testing a video camera was placed behind the horizontal bar and recorded each trial. A schematic representation of the experimental setup can be seen in Figure
Each participant was seated at the workspace where the objects were presented. Using the horizontal bar as a guide, participants were instructed to lift and balance each object using a pincer grip with the index and thumb of their left hand. After the object was lifted to the horizontal bar, participants returned the object to the table and removed their hand from it before another trial began. It was emphasized that if the object was imbalanced, they should not compensate by tightly pinching the object or rotating their wrist during or at the end of each lift. Task instructions were demonstrated using the evenly weighted practice cylinder. Participants were then requested to practice the task procedure using the same cylinder. Once participants successfully completed the movement they were presented the unevenly weighted practice cylinder and repeated the process. After it was evident that participants understood the procedure, the main task was started. During the main task, to ensure each participant had the same experience with the object, they were asked to lift and balance each object five times before being presented the next object. In each block, objects were presented in a random order. Overall, there were five testing blocks in which participants saw each object once; including each individual trial, participants lifted each object 25 times, totalling 125 trials. The video camera recorded participants completing each trial.
Task performance across each condition was initially compared between each control group (healthy and non-apraxics) using a two-way mixed model ANOVA exploring OBJECT (memory-associated; visual-spatial cue; neutral-control) × GROUP (Healthy vs. Non-apraxic controls) to rule out differences across control groups. Each apraxic patient was then compared to the control groups separately using modified
Firstly, in order to analyze the video footage, photo snapshots were created when participants were at the maximal point of object lift. From each snapshot, the “point of grasp” was measured based on the midpoint position of the index finger along the object (from right to left). Grasps were considered accurate depending on whether the object was successfully balanced and an appropriate point of grasp was applied to compensate for the objects weight distribution. This ensured that participants were accurate due to adjusting their grasp-point along the object, as opposed to applying greater grip force or by rotating their wrist during each lift. If the location of an individual’s grasp was greater than two standard deviations from the “optimum” point of grasp (OP) to compensate for weight distribution, it was marked as inaccurate. The optimum point of grasp was measured for each object based on healthy control participants mean point of grasp for the fifth trial across all blocks.
Grasp accuracy was compared between Trial 1 and Trial 5 across blocks. Performance change across trials would indicate whether apraxic patients’ performance improved with repeated grasps of the same object. To compare performance, accuracy was first weighted; accurate grasps in early trials (e.g., Trial 1) received a greater weighting compared to accurate grasps in later trials (e.g., Trial 5). This reflected the extent to which performance was driven by trial-and-error or learning each objects weight distribution. Inaccurate grasps were given a negative score: fewer points were deducted when grasps were inaccurate in early trials and greater points deducted when performing inaccurately in later trials. These reflected the extent to which participants failed to adapt their grasp based on each objects’ weight distribution with repeated grasps of the same object (see Table
1 | 2 | 3 | 4 | 5 | |
---|---|---|---|---|---|
Correct | 5 | 4 | 3 | 2 | 1 |
Incorrect | −1 | −2 | −3 | −4 | −5 |
Correct | 5 | 4 | 3 | 2 | 1 |
Incorrect | −1 | −2 | −3 | −4 | −5 |
Accuracy change (TC) = (block 1–5 average scoretrial 1/maximum scoretrial 1) − (block 1–5 average scoretrial 5/maximum scoretrial 5).
Using the same calculation, performance across blocks was assessed by comparing the average accuracy across trials between Block 1 and Block 5. Performance change across blocks would confirm whether apraxic patients applied what they had learned in previous blocks when each object was reintroduced. As with trial data, performance across blocks was weighted using positive and negative scores. In early blocks, participants received greater points for accurate grasps and fewer points were deducted for inaccurate grasps, whereas in later blocks participants received fewer points for accurate grasps and more points were deducted for inaccurate grasps. Scores were transformed into proportions of the maximum score before accuracy in Block 5 was deducted from accuracy in Block 1.
Notably during testing, non-apraxic patients BH and JS completed only four testing blocks due to experiencing fatigue when lifting the objects several times. The same calculation applied to the final block was instead applied to Block 4 for these patients.
In order to confirm whether apraxic patients utilized memory-associations or visual-spatial cues regarding weight distribution when balancing each object, performance change across trials and across blocks were assessed. Points of grasp for each object were used as a guide to evaluate grasp behavior.
An initial two-way mixed model ANOVA exploring OBJECT (memory-associated; visual-spatial cue; neutral-control) × GROUP ruled out differences in performance change across Trials in healthy and non-apraxic controls. Non-significant main effects confirmed that performance was comparable across control groups (GROUP:
Despite variances in performance change for the neutral-control object, healthy and non-apraxic controls consistently grasped the object close to the optimum grasp-point (OP = 13.18 cm). Examining grasp-point behavior of controls across all three conditions, both groups initially grasped closer to the center of each object in Trial 1, but by Trial 5 were ≤1.32 cm from the optimum grasp-point for each object. Observing individual scores for performance change over trials (TC) confirms that each control participant appropriately adapted their grasp-point over repeated lifts to account for the weight distribution of each object. Of note, non-apraxic control participant JS did not perform as efficiently as the other non-apraxic patients in the memory-associated and visual-spatial cue conditions. However, she was still markedly more accurate than AH and GW. Patient JS also performed at ceiling during the language comprehension test and apraxia screening indicating that her performance was not applicable to poor comprehension or apraxia. Instead, her performance may be more attributable to her age; JS was the oldest participant (91) and testing had to be terminated after the fourth test block as she became fatigued. Together, these findings indicate that healthy and non-apraxic controls effectively utilize both memory-associated and visual-spatial cued information to improve performance when repeatedly lifting each object (see Table
Change across trials (TC) | Change across blocks (BC) | |||||
---|---|---|---|---|---|---|
PT | Memory-associated | Visual-spatial cue | Neutral-control | Memory-associated | Visual = spatial cue | Neutral-control |
SG | −0.48 | −0.24 | −0.24 | −0.36 | 0.48 | 0 |
TY | 1.2 | 0.6 | 0 | 0 | 0.24 | 0 |
DF | −0.48 | −0.12 | 0 | −0.24 | −0.12 | 0 |
WM | −0.84 | −0.165 | −0.48 | 2.16 | 0.28 | 1.2 |
MB | −0.6 | −0.84 | −0.48 | −0.24 | 0.12 | 1.92 |
TM | −0.96 | −0.24 | −0.48 | 0.36 | −0.12 | 0 |
DJ | −0.12 | 0.36 | −0.72 | 0 | −0.36 | 1.2 |
JS | 1.8 | 1.65 | 0 | 1.8 | 1.65 | −1.5 |
BH | −0.9 | −0.6 | −0.6 | −1.99 | −1.11 | 1.5 |
−0.153 | 0.045 | −0.333 | 0.166 | 0.118 | 0.48 | |
AH | 4.8 | 2.52 | 0 | 4.8 | 3.24 | 0 |
GW | 4.8 | 4.8 | 0 | 4.8 | 4.2 | 0 |
JA | −0.84 | 0.36 | −0.24 | 0.48 | −0.72 | 0 |
Point of Grasp (distance from OP) | ||||||||||
---|---|---|---|---|---|---|---|---|---|---|
Memory-associated | Visual-spatial cue (Dot) | Neutral-control | ||||||||
Left weighted (OP = 20.18) | Right weighted (OP = 6.30) | Left weighted (OP = 19.85) | Right weighted (OP = 6.29) | Evenly weighted (OP = 13.18) | ||||||
1 | 5 | 1 | 5 | 1 | 5 | 1 | 5 | 1 | 5 | |
AH | 11.50 (8.69) | 12.55 (7.63) | 12.00 (−6.83) | 11.35 (−6.18) | 11.75 (8.10) | 12.00 (7.85) | 12.00 (−5.70) | 11.10 (−4.80) | 11.70 (1.48) | 11.55 (1.63) |
GW | 13.70 (6.49) | 15.00 (5.18) | 13.60 (−8.43) | 13.55 (−8.38) | 13.65 (6.20) | 13.95 (5.90) | 12.95 (−6.65) | 13.00 (−6.70) | 13.30 (−0.12) | 13.60 (−0.42) |
JA | 17.10 (3.09) | 21.30 (−1.12) | 15.70 (−10.53) | 2.55 (2.62) | 20.70 (−0.85) | 18.54 (1.31) | 5.55 (0.75) | 2.10 (4.20) | 14.30 (−1.12) | 12.85 (0.33) |
Healthy | ||||||||||
Controls | 14.09 (6.10) | 20.21 (−0.03) | 11.53 (−6.36) | 5.15 (0.02) | 17.48 (2.37) | 19.84 (0.01) | 9.60 (−3.31) | 6.30 (0) | 13.48 (−0.29) | 13.18 (0.01) |
Non-apraxics | 13.48 (6.80) | 19.04 (1.22) | 11.26 (−6.07) | 5.62 (−0.52) | 16.45 (3.45) | 19.05 (0.89) | 9.23 (−3.01) | 5.88 (0.33) | 11.91 (1.33) | 12.57 (0.58) |
AH | 12.10 (8.08) | 13.45 (7.30) | 11.70 (−6.53) | 12.60 (−7.43) | 11.80 (8.05) | 12.55 (7.30) | 11.75 (−5.45) | 11.50 (−5.20) | 11.70 (1.48) | 11.70 (1.48) |
GW | 15.65 (4.53) | 15.40 (4.45) | 13.95 (−8.78) | 14.35 (−9.18) | 14.10 (5.75) | 15.40 (4.45) | 13.50 (−7.20) | 13.90 (−7.60) | 12.70 (0.48) | 14.95 (−1.77) |
JA | 20.85 (−0.67) | 20.80 (−2.10) | 6.55 (−1.38) | 4.80 (0.37) | 6.74 (13.11) | 21.95 (−2.10) | 5.70 (0.60) | 2.20 (4.10) | 12.60 (0.58) | 12.65 (0.53) |
Healthy controls | 17.98 (2.20) | 19.32 (−0.04) | 7.43 (−2.25) | 6.28 (−1.11) | 16.66 (3.19) | 19.89 (−0.04) | 7.80 (−1.51) | 6.58 (−0.28) | 12.86 (0.32) | 12.99 (0.19) |
Non-apraxics | 16.93 (3.25) | 18.96 (0.50) | 8.86 (−3.39) | 5.21 (−0.58) | 16.47 (3.39) | 19.77 (0.50) | 7.69 (−1.39) | 5.37 (−0.01) | 13.10 (0.08) | 11.37 (1.32) |
Single case
Observing the average grasp-points for both the memory-associated and visual spatial cue conditions, patient AH maintained a point of grasp towards the center of each object (from 11.10 cm to 13.45 cm). These grasps were at least 4.8 cm from the optimum grasp-point to compensate for weight distribution of each object. Unlike control groups, patient AH did not adjust her grasp towards the weighted end of across trials.
As this patient did not adjust her grasp away from the midpoint, when grasping the neutral-control object AH’s performance change was comparable to both healthy controls (
Performance of patient GW mirrored that of patient AH. Performance change over trials was worse than healthy and non-apraxic controls when grasping unevenly weighted objects in both the memory-associated and visual-spatial cue conditions: for all comparisons
Apraxic patient JA’s performance change across trials was comparable to both healthy and non-apraxic controls for the memory-associated and neutral-control conditions (
Statistically this behavior was not so much apparent in the average grasp-point variance itself but in the standard deviation of her grasp-point variance. On the average grasp-point variance JA showed marginally significant differences on the memory associated condition (
Non-significant main effects and interactions from the two-way mixed model ANOVA confirmed that performance change across Blocks was comparable between control groups: OBJECT,
Accuracy change was worse than both healthy and non-apraxic controls during the memory-associated and visual-spatial cue conditions (for all comparisons
As before, patient AH’s performance change was comparable to healthy (
Similarly, during the memory-associated and visual-spatial cue conditions patient GW performed worse than healthy controls and non-apraxics; for all comparisons
Mirroring patient AH, when grasping the neutral-control object, GW’s performance change was equivalent to healthy (
Across all three conditions (memory-associated/visual-spatial cue/neutral-control) patient JA’s performance change was comparable to controls (
To assess whether apraxic patients successfully integrate stored knowledge of objects into action plans, participants were required to learn different weight distributions when lifting and balancing objects using a pincer grip. Over two conditions, each objects’ weight distribution was indicated by either a memory-associated cue (object color) or visual-spatial cue (visible dot over the weighted end). If apraxic patients fail to incorporate stored information into their grasp, we expected that patients might disregard the location of the objects’ center of mass and instead over-rely on visual information, resulting in more centrally oriented grasps based on object structure. The experiment was designed to examine whether patients could learn to grasp the weighted objects accurately when given a meaningful visual-spatial cue indicating the object weight distribution, which would result in increasingly accurate grasps over time if this higher-level information was successfully integrated.
Performance change across trials (TC) and across blocks (BC) in the neutral-control screening condition confirmed that all apraxic patients (AH, GW, and JA) successfully grasped and balanced the evenly weighted object, eliminating the possibility any confounds such as hemispatial neglect or impaired task comprehension might be impacting their performance in the experimental conditions. Comparable to healthy and non-apraxic controls, during consecutive grasps of the neutral-control object (TC) and when grasping the object as it was reintroduced in later blocks (BC), apraxic patients’ central grasp-points remained close to the optimum point of grasp to compensate for weight distribution. Accurate grasping performance during the neutral-control condition indicates that apraxic patients can successfully manipulate objects when the weight distribution is indicated by the objects’ structure (symmetrical cylinder).
Although patient JA’s performance change was within the normal range (see below for a discussion of JA’s pattern of results) during a majority of the memory-associated and visual-spatial cue conditions, patients AH and GW failed to update their grasp-point when the objects were unevenly weighted in both conditions. For both the memory-associated and visual-spatial cue conditions, patient AH and GW maintained a central grasp-point during recurrent trials with the same object (TC) or when the objects were reintroduced in later blocks (BC). Failure to compensate for load torque by reorienting grasps towards the center of mass suggests that these apraxic patients failed to integrate acquired knowledge regarding objects into action plans. Inaccurate grasp-points persisting into the final test block was particularly representative of this. Paired with unimpaired behavior in the neutral-control condition, grasp performance of patients AH and GW suggests an over-reliance on the structural properties afforded by the object. Maintained central grasp-points in the memory-associated and visual-spatial cue conditions perhaps indicate that AH and GW continually referred to structural properties afforded by the object to guide their grasp behavior and did not benefit from either a meaningful visual-spatial cue or symbolic cue of weight distribution.
Patient AH and GW’s performance is compatible with previous research indicating that in addition to impaired perception of skilled object-use (Buxbaum and Saffran,
Interestingly, both patients AH and GW did not appear to benefit at all from the “dot” cue in the visual-spatial cue condition, and there was no evidence of learning. In healthy populations when an object is asymmetrically weighted, grasp-points typically migrate towards the weighted end, particularly when visual cues indicate where the center of mass is located (Endo et al.,
It is possible that a visual cue, such as a dot, is not ecologically meaningful and subsequently requires more explicit learning. This differs from implicit visual geometric cues of shape and size that are ecologically meaningful (Gentile,
Additionally, it was somewhat surprising that patients’ AH and GW did not benefit from short-term sensorimotor feedback to improve grasp performance during subsequent trials within a block (TC). Attributed to the bilateral dorsal stream, rapidly decaying sensorimotor memory is formed and updated with repeated grasps of the same object (Bursztyn and Flanagan,
Interestingly, patient JA’s performance change was comparable to control groups in all conditions, except when compared to healthy controls during repeated grasps (TC) of the visual-spatial cue objects. However, further analyses of grasp-point indicate that patient JA did indeed struggle to apply knowledge-based information or visual-spatial cues in learning to grasp the weighted objects. Exploring JA’s behavior when grasping visual-spatial cued objects, a positive score for accuracy change over trials indicates that JA continued to make errors to the final trial. Although these errors were only minor in contrast to patient AH and GW who consistently failed to adjust their grasp-point according to weight distribution, when examining individual participants’ performance change none of the non-apraxic patients or healthy controls failed to adapt their grasp-point over repeated lifts (TC) and when the objects were reintroduced (BC). Therefore it is possible that apraxic patient JA used compensatory mechanisms to improve performance. Patient JA’s variable grasp behavior also suggests that she may be maintaining a trial-and-error procedure throughout the experiment. In particular, when grasping specific objects within the memory-associated and visual-spatial cue conditions, patient JA’s grasp-point deviated further from the optimum point of grasp to compensate for object weight distribution in later trials and when the objects were reintroduced, whereas control participants grasps moved closer to the optimum grasp-point. Likewise, patient JA’s point of grasp was grossly variable from Block 1–5; JA adjusted her grasp-point by almost 20 cm in both the memory-associated and visual-spatial cue conditions. This behavior seemed to demonstrate a more subtle manifestation of the deficit in the integration of visible and known object properties that results in more changeable grasp accuracy.
These subtle effects in JA were in line with the behavior she displayed. JA, a young and highly motivated patient, performed the task slowly and deliberately. She appeared more aware of her deficit than the other patients. Perhaps this due to the fact that she was aware of her apraxic symptoms that included actual object-use (evident in standard apraxia screening). If this is the case, JA is more likely to compensate for her impairment resulting in improved grasping performance compared to the other apraxic patients. Although patient AH has a similar lesion to JA, she inevitably will have been less aware of her apraxic symptoms that did not include actual object-use. Likewise, GW demonstrated more severe apraxic errors across the screening tasks and may be less able to effectively compensate for his impairment. No compensative strategies in performance of the experimental task were apparent in AH or GW who performed the task very quickly, immediately reaching for the object at the start of each trial and rapidly lifting each object before returning it to the table. In contrast, JA showed awareness of difficulty with the task, commenting on completion that she tried to apply strategies: she said that when the object was placed in the testing area, she observed whether one end of the object landed on the table first as a potential clue to its weight distribution. Although the availability of such cues were avoided through careful placement of each object, it may be beneficial to occlude participants’ view when objects are placed on the table. However, it was felt that the presence of each object during testing ensured that participants were aware that each object reintroduced in later blocks was the same as those seen previously. Finally, the less gross errors of patient JA on the grasping task compared to AH and GW cannot be attributed to better comprehension, as JA scored the least in the language comprehension test. Likewise, JA did not suffer from milder apraxic symptoms; as described, patient GW demonstrated the more severe apraxic symptoms whereas JA’s apraxic behavior was comparable to AH.
Rather than ventro-dorsal processing remaining intact in patient JA, it is believed that through her careful performance, she managed to assemble compensatory strategies, even when weight distribution was afforded by a high-level visual-spatial cue. Appropriate performance when behavior is delayed in apraxic patients suggests that stored knowledge is maintained, but difficult to access. As described, accurate memory-driven reach and grasp performance is observed when apraxic patients pick up basic blocks based on simple size and distance information (Ietswaart et al.,
Although the design of the current study delayed reach-to-grasp action between trials by requiring participants to return their hand to the table before beginning another grasp movement, the duration of this delay was not controlled. Further investigation is required to confirm whether delay between reaching and grasping can reduce performance errors when balancing novel objects. It is probable that such compensatory strategies may rely on critical brain structures being intact; JA presented with frontal lesions that implicate white matter whilst parietal regions remain undamaged (as was the case in AH). In contrast, GW’s lesion implicates temporal and parietal regions of the left hemisphere suggesting that the critical juncture between the ventral and dorsal pathways may be compromised (Rizzolatti and Matelli,
In conclusion, apraxia was associated with a disrupted ability to utilize memory-associated or visual-spatial cued information indicating weight distribution. Specifically, patient AH and GW failed to successfully incorporate memory-associated information where weight distribution was indicated by the objects color, and visual-spatial cued information in the form of a dot cue over the objects weighted. Grasps were inaccurate during repeated lifts and when the objects were reintroduced. A third apraxic patient (JA) seemed to compensate for these difficulties but still showed performance errors that may be attributable to a more subtle impairment. These results indicate that apraxia impairs the ability to utilize meaningful visual-spatial cue or symbolic memory-associated cues when grasping objects to achieve specific action goals. Crucially, the abnormal grasping behavior in these apraxic patients suggests that integration of visible and known object properties attributed to the ventro-dorsal stream is impaired. Not only does disruption to ventro-dorsal processing impair use of familiar objects, but also these results would predict that apraxia is associated with difficulty learning to manipulate new objects.
CE, conception and design of the research task; acquisition, analysis and interpretation of the data; drafting the manuscript and final editing. MGE, contribution to the conception of the task, critically revising and editing the manuscript, and final approval of the manuscript. LJT, contribution to the conception of the task, final approval of the manuscript version to be published. MI, substantial contribution to the conception and design of the research task, interpretation of the data and critically revising and editing the manuscript.
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
This study was funded by Northumbria University. We would like to thank the individuals who took part in the study, the local NHS hospitals and rehabilitation centres in the North East of England where many were recruited, and in particular the responsible clinicians Dr. David Bruce, Dr. Tim Cassidy, Dr. Akif Gani, and Dr. Chris Price and their teams.
1
2