Neural representation of hand kinematics during prehension in posterior parietal cortex of the macaque monkey

Abstract

Studies of hand manipulation neurons in posterior parietal cortex of monkeys suggest that their spike trains represent objects by the hand postures needed for grasping or by the underlying patterns of muscle activation. To analyze the role of hand kinematics and object properties in a trained prehension task, we correlated the firing rates of neurons in anterior area 5 with hand behaviors as monkeys grasped and lifted knobs of different shapes and locations in the workspace. Trials were divided into four classes depending on the approach trajectory: forward, lateral, and local approaches, and regrasps. The task factors controlled by the animal-how and when he used the hand-appeared to play the principal roles in modulating firing rates of area 5 neurons. In all, 77% of neurons studied (58/75) showed significant effects of approach style on firing rates; 80% of the population responded at higher rates and for longer durations on forward or lateral approaches that included reaching, wrist rotation, and hand preshaping prior to contact, but only 13% distinguished the direction of reach. The higher firing rates in reach trials reflected not only the arm movements needed to direct the hand to the target before contact, but persisted through the contact, grasp, and lift stages. Moreover, the approach style exerted a stronger effect on firing rates than object features, such as shape and location, which were distinguished by half of the population. Forty-three percent of the neurons signaled both the object properties and the hand actions used to acquire them. However, the spread in firing rates evoked by each knob on reach and no-reach trials was greater than distinctions between different objects grasped with the same approach style. Our data provide clear evidence for synergies between reaching and grasping that may facilitate smooth, coordinated actions of the arm and hand.

Fig. 1.

Kinematic drawings of forward (A), lateral (B), and local (C) approach to the large round knob by monkey H17094 using the right hand. Outlines of the hand and test objects were traced from sequential video frames and superimposed to provide a time series of actions performed on individual trials of the prehension task. Numbers to the right in each panel indicate the time codes of the traced images (min:s:frame) recorded at 30 frames per second (fps). Each trial began with the animal viewing cues on the computer monitor (dashed green lines); the cued knob is denoted in the figure by an asterisk. The hand trajectory toward the knob was smooth and direct regardless of the reach direction. Note the common hand preshaping, contact, and grasp postures used in these trials. Unit H17094-129-2, tactile receptive fields on the tips of digits 2–5 and the thumb.

Fig. 2.

Hand kinematics used by monkey N18588 during task performance with the left hand. Same format as that in Fig. 1. The forward (A), lateral (B), and local (C) approaches used by this animal were similar to those for the other animal, but the grasp postures differed. Monkey N18588, Track 313, clip 7, right hemisphere; passive receptive fields were not determined in this session.

Fig. 3.

Spike rasters comparing responses of an area 5 neuron in monkey H17094 to the four approach styles. Each of the raster panels is aligned to contact, subdivided by knob location and shape, and ordered chronologically within each style. Colored markers in the rasters show the onset times of the task stages on each trial: 1. Approach (gold); 2. Contact (red); 3. Grasp (magenta); 4. Lift (dark blue); 5. Hold (light blue); 6. Lower (dark green); 7. Relax (green); 8. Release (cyan). Forward (A) and lateral (B) approach trials evoked higher firing rates and longer duration responses than local grasps (C) and regrasps (D). Spike trains evoked by individual knobs acquired with the same style resembled each other. Regrasp trials in which the animal used the “ulnar grasp” posture are marked with a cyan bar to the left of the raster in D. Unit H17094-131-3.2, tactile receptive field located on the glabrous and hairy skin of the hand and digits.

Fig. 4.

Superimposed spike density plots (left) and average firing rates per task stage ± SE (right) compiled for the neuron in Fig. 3. Responses in the spike density plots are aligned to contact and grouped by approach style (A) and object shape (B). Markers above the spike density graphs show the mean onset times of the task stages averaged across all trials of the stated class; same color codes per stage as those in Fig. 3. The top-to-bottom listing of the knobs in the key corresponds to their medial-to-lateral positions on the shape box. P values in the average firing rate graphs indicate the selectivity of the neuron for approach style (A) and object shape (B) as determined by repeated-measures ANOVA; distinctions between approach styles were stronger than those between the various objects.

Fig. 5.

Selectivity of an area 5 neuron recorded in monkey N18588 for approach style and object properties. A–D: rasters of all 107 trials of this neuron are grouped by approach style, and subdivided by knob shape and location. Same format as Fig. 3. Forward and lateral approach styles evoked the highest firing rates and longest duration responses. Regrasps (D) occurred most frequently at the site lateral to the active arm (knob 1) and on only one trial at the medial and midline sites (knobs 3 and 4). E: spike density plots for the 4 approach styles. F: average rate graphs for approach style (left) and knob shape (right).

Fig. 6.

Mean stage durations (±SE) for the 4 approach styles are similar in the 2 animals. The reach style modified the duration of the approach, contact, and hold stages but the grasp and lift stages lasted the same time regardless of how the knob was acquired.

Fig. 7.

Population mean normalized firing rates per stage plotted as a function of approach style (A), object shape (B), and object location (C) for the 75 neurons studied in the 2 animals. P values in each panel indicate the selectivity for style, shape, or location as determined by repeated-measures ANOVA; the significance of interaction effects on firing rates across the task stages is also noted. Top panels: trials grouped by approach style (A) showed greater disparity than those grouped by object shape (B) or location (C). Bottom panels: approach styles in the population were grouped into reach trials (forward and lateral approach, solid lines) and no-reach trials (local approach and regrasp, dashed lines). Reach trials evoked significantly greater responses than no-reach trials during the approach, contact, grasp, and lift stages, as well as in the pretrial interval. The distinction between reach and no-reach trials was greater than that of the object shape (B) or location (C) within each style.

Fig. 8.

Kinematic drawings demonstrating clumsy grasps during visual block trials; same format as that in Fig. 1. An opaque plate placed below the chin blocked view of the workspace and the hand, but did not physically impede reaching or grasping movements. A: lateral approach trial in which the animal palpated the top surface and fumbled with the knob before grasping it. B: forward approach trial in which the animal slid the ulnar margin of the hand along the top of the shape box and used an abnormally large grip aperture during approach. The left hand rested on the medial rectangle, thereby providing proprioceptive cues about the relative locations of the knobs in the workspace. Unit H17094-131-3, clip 7; neural responses from this cell are shown in Fig. 9A.

Fig. 9.

Spike density plots (left), average firing rate graphs (center), and mean stage duration (right) comparing sighted and blocked reach trials for 3 neurons in monkey H17094. A: neuron favoring sighted trials; same neuron as that in Figs. 3, 4, and 8. B: neuron favoring blocked trials. It also responded to passive stroking of the dorsum of digit 3 (proximal phalanx) and passive flexion of the metacarpophalangeal joints of digits 2–5. C: neuron that did not distinguish the 2 trial types; receptive field not identified. The mean duration of stage 2 (contact) was significantly longer on blocked trials in all 3 neurons.

Fig. 10.

A: population mean normalized firing rates per stage for the 25 neurons studied as a function of visual condition during reach (R) and no-reach (NR) trials. Firing rates were slightly higher during sighted trials than when vision of the workspace was blocked, but the difference was not significant. B: the mean stage duration in sighted and blocked trials differed only during the contact stage as the hand was positioned for grasp. For clarity, timing data are shown only for the reach trials.