The impact of left hemisphere stroke on force control with familiar and novel objects: neuroanatomic substrates and relationship to apraxia

Abstract

Fingertip force scaling for lifting objects frequently occurs in anticipation of finger contact. An ongoing question concerns the types of memories that are used to inform predictive control. Object-specific information such as weight may be stored and retrieved when previously encountered objects are lifted again. Alternatively, visual size and shape cues may provide estimates of object density each time objects are encountered. We reasoned that differences in performance with familiar versus novel objects would provide support for the former possibility. Anticipatory force production with both familiar and novel objects was assessed in six left hemisphere stroke patients, two of whom exhibited deficient actions with familiar objects (ideomotor apraxia; IMA), along with five control subjects. In contrast to healthy controls and stroke participants without IMA, participants with IMA displayed poor anticipatory scaling with familiar objects. However, like the other groups, IMA participants learned to differentiate fingertip forces with repeated lifts of both familiar and novel objects. Finally, there was a significant correlation between damage to the inferior parietal and superior and middle temporal lobes and impaired anticipatory control for familiar objects. These data support the hypotheses that anticipatory control during lifts of familiar objects in IMA patients are based on object-specific memories and that the ventro-dorsal stream is involved in the long-term storage of internal models used for anticipatory scaling during object manipulation.

Fig. 1

Load force rate (LFR) traces across time for Trial 1 with familiar objects for two controls, two LCVA participants without ideomotor apraxia (IMA), and two LCVA participants with IMA. Below each LFR trace is a depiction of object position to indicate the point at which object lift-off was achieved. Controls and LCVA appropriately scaled LFR based on object weight for familiar objects wherein heavier objects elicited higher LFRs. Furthermore, LFRs were primarily single-peaked and the maximumpeak value was achieved before the object is lifted off the table, indicating a smooth application of load force that precedes and anticipates sensory feedback. In contrast, IMA participants had poorly differentiated and incorrectly scaled LFRs based on object weight. They tended to generate multi-peaked waveforms with a low first peak before object lift-off and a second maximum peak after lift-off once sensory feedback regarding object weight was available. Other force fluctuations were noticeable in the IMA participants, including large negative load forces prior to lift-off, suggesting an attempt to stabilize the grasp, and multiple sub-peaks while holding the object aloft, indicating difficulty maintaining the grip.

Fig 2

Somers’ Dmeasure of association between real object weight and fingertip force. Each participant’s force rate is plotted by object and objects are ordered by ascending weight from left to right along the x-axis. Given that the x-values are ordered, Somers’ D is the difference between concordant and discordant pairs, divided by the number of concordant, discordant and tied pairs for the x-value. (A) Control LFR for familiar objects on Trials 1 and 5. (B) Patient LFR for familiar objects on Trials 1 and 5. Apraxics are demarcated by dark filled circles and non-apraxics by open circles. (C) Control GFR for novel objects on Trials 1 and 5. (D) Control LFR for novel objects on Trials 1 and 5. (E) Patient GFR for novel objects on Trials 1 and 5. (F) Control LFR for novel objects on Trials 1 and 5.

Fig. 3

A scatterplot and regression line showing the relationship between load force rate (LFR) Distance for Trial 1 with familiar objects and the gesture to sight (GTS) test of ideomotor apraxia. R-sq.=0.67

Fig. 4

(A) Overlay maps of all patients lesions (n=6) on axial slices (slice location indicated by z-coordinate) and a 3D cortical rendering of the left hemisphere. Colors ranging from dark blue to light green indicate the number of patients who share the same lesion location, where the darkest color indicates lesions in only one patient and the lightest color indicates lesions in all six patients. (B) Subtraction maps of lesions of most impaired (n=3) versus least impaired (n=3) stroke participants based on scores on load force rate (LFR) Distance Trial 1 with familiar Objects. Colors ranging from yellow to red indicate lesion loci damaged in more “most impaired” than “least impaired” participants (yellow=damaged in 3 “most impaired” and 0 “least impaired”; posterior superior temporal and inferior parietal lobes). Colors ranging from light blue to dark blue indicate regions more frequently damaged in “least impaired” than “most impaired” participants. Purple indicates regions that did not distinguish between groups (difference of 0).

Fig. 5

Scatterplots and regression lines showing the relationship between load force rate (LFR) Order Trial 1 for familiar objects and number of voxels damaged in brain regions of interest. STG=superior temporal gyrus; IPL=inferior parietal lobe; TO=posterior temporal-occipital; MTG=middle temporal gyrus.

Fig. 6

Experimental setup. (A) Familiar object: In this case, videotape, with a Polhemus position sensor (Polhemus Fastrack, Colchester, VT) attached being lifted from a platform attached to a 6 DOF force transducer (Nano17; ATI Industrial Automation, Garner, NC, USA), placed horizontally, acting as a load cell. (B) Novel objects: One of three geometric shaped objects (Cube shown) attached to a grip device consisting of two parallel 6 DOF force transducers with contact surfaces made from 200 grit sandpaper. A position sensor is attached. Familiar and novel objects were lifted to a height of 6 cm to be aligned to a vertical marker.