Apostolos P. Georgopoulos

Cortical mechanisms related to the direction of two-dimensional arm movements: relations in parietal area 5 and comparison with motor cortex

SummaryThe relations between the direction of two-dimensional arm movements and single cell discharge in area 5 were investigated during 49 penetrations into the superior parietal lobule of 3 monkeys. A significant variation of cell discharge with the direction of movement was observed in 182 of 212 cells that were related to arm movements. In 151/182 of these cells the frequency of discharge was highest during movements in a preferred direction, and decreased in an orderly fashion with movements made in directions farther and farther away from the preferred one; in 112/151 cells this variation in discharge was a sinusoidal function of the direction of movement. Preferred directions differed for different cells so that directional tuning curves overlapped partially. These results are similar to those described for cells in the motor cortex (Georgopoulos et al. 1982): this suggests that directional information may be processed in a similar way in these structures.Many cells in area 5 changed activity before the onset of movement, and several did so before the earliest electromyographic changes (63% and 35%, respectively, of the cells that showed an increase in activity with movements in the preferred direction). However, the distribution of onset times of the parietal cells lagged the corresponding one of the motor cortical cells by about 60 ms. This suggests that the early changes observed in the parietal cortex might represent a corollary discharge from the pre-central motor fields, whereas later activity might reflect peripheral as well as central events.

Cognitive spatial-motor processes. 1. The making of movements at various angles from a stimulus direction.

SummaryNaive human subjects (N=18) were asked to move a manipulandum on a plane in directions other than going straight towards a visual stimulus. They were instructed verbally to generate a movement at an angle from a stimulus direction which varied in 2-dimensional (2-D) space from trial to trial in a pseudorandom fashion. Each subject performed eight sets of twenty consecutive trials: one for moving in the stimulus direction and seven for moving in directions at an angle from it. The angles were 5, 10, 15, 35, 70, 105 and 140°. Nine subjects were instructed to move in the clockwise (CW) departure and 9 to move in either (EI) the clockwise or the counterclockwise (CCW) departure, as they wished. The direction of the movement in 2-D space and the reaction time (RT) were measured. The mean angle achieved in a given set overshot the instruction angle, especially in the lower range (5–35°). The reaction time, (RTΘ), of movements made at an angle from the stimulus direction showed two kinds of change: first, a step increase from the reaction time, RT0, of movements in the stimulus direction, and second, superimposed upon it, a linear increase with the amplitude of the angle. The slope of the line was similar for the CW (2.37 ms/degree) and the EI case (2.28 ms/degree), but the step increase (y-intercept) for the EI case (84 ms) was substantially less than that of the CW case (155 ms). The linear increase of the RT with angle is compatible with the idea that performance in the task may involve a mental rotation of the imagined movement vector about its origin. The rotation would begin from the stimulus direction and end when the required angle is judged to have been reached; in addition, corrections of this angle at the end of the rotation could be made. The slope of 2.37 ms/degree observed in the CW case would correspond to a rotation rate of 422 degrees/s. The finding of a similar rate for the EI case indicates a similarity in strategy with regard to achieving a desired angle. In contrast, the lower intercept observed for the EI case suggests significant savings in processing information which is unconstrained with regard to angular departure. Assuming this model of internal motion, we analyzed the amplitude-accuracy relations using Fitts (1954) approach to real movements. In accordance with Fitts law, we found that the increase in RT, considered as a mental movement time, was a linear function of task difficulty which was calculated from the angle achieved and its variability. This indicates that Fitts law holds for the hypothesized rotatory motion of the imagined movement vector, and that both real and imagined movements might be governed by similar amplitude-accuracy relations.

Motor Area Activity During Mental Rotation Studied by Time-Resolved Single-Trial fMRI

The functional equivalence of overt movements and dynamic imagery is of fundamental importance in neuroscience. Here, we investigated the participation of the neocortical motor areas in a classic task of dynamic imagery, Shepard and Metzlers mental rotation task, by time-resolved single-trial functional Magnetic Resonance Imaging (fMRI). The subjects performed the mental-rotation task 16 times, each time with different object pairs. Functional images were acquired for each pair separately, and the onset times and widths of the activation peaks in each area of interest were compared to the response times. We found a bilateral involvement of the superior parietal lobule, lateral premotor area, and supplementary motor area in all subjects; we found, furthermore, that those areas likely participate in the very act of mental rotation. We also found an activation in the left primary motor cortex, which seemed to be associated with the right-hand button press at the end of the task period.

Parallel processing of serial movements in prefrontal cortex.

A key idea in Lashleys formulation of the problem of serial order in behavior is the postulated neural representation of all serial elements before the action begins. We studied this question by recording the activity of individual neurons simultaneously in small ensembles in prefrontal cortex while monkeys copied geometrical shapes shown on a screen. Monkeys drew the shapes as sequences of movement segments, and these segments were associated with distinct patterns of neuronal ensemble activity. Here we show that these patterns were present during the time preceding the actual drawing. The rank of the strength of representation of a segment in the neuronal population during this time, as assessed by discriminant analysis, predicted the serial position of the segment in the motor sequence. An analysis of errors in copying and their neural correlates supplied additional evidence for this code and provided a neural basis for Lashleys hypothesis that errors in motor sequences would be most likely to occur when executing elements that had prior representations of nearly equal strength.

Static spatial effects in motor cortex and area 5: Quantitative relations in a two-dimensional space

SummaryWe describe the relations between active maintenance of the hand at various positions in a two-dimensional space and the frequency of single cell discharge in motor cortex (n = 185) and area 5 (n = 128) of the rhesus monkey. The steady-state discharge rate of 124/185 (67%) motor cortical and 105/128 (82%) area 5 cells varied with the position in which the hand was held in space (“static spatial effect”). The higher prevalence of this effect in area 5 was statistically significant. In both structures, static effects were observed at similar frequencies for cells that possessed as well as for those that lacked passive driving from the limb. The results obtained by a quantitative analysis were similar for neurons of the two cortical areas studied. It was found that of the neurons with a static effect, the steady-state discharge rate of 78/124 (63%) motor cortical and 63/105 (60%) area 5 cells was a linear function of the position of the hand across the two-dimensional space, so that the neuronal “response surface” was adequately described by a plane (R2 ≥ 0.7, p < 0.05, F-test in analysis of variance). The preferred orientations of these response planes differed for different cells. These results indicate that individual cells in these areas do not relate uniquely a particular position of the hand in space. Instead, they seem to encode spatial gradients at certain orientations. A unique relation to position in space could be signalled by the whole population of these neurons, considered as an ensemble. This remains to be elucidated. Finally, the similarity of the quantitative relations observed in motor cortex and area 5 suggests that these structures may process spatial information in a similar way.

Sequential activity in human motor areas during a delayed cued finger movement task studied by time-resolved fMRI

ACTIVITY in the human primary motor cortex, the premotor cortex and the supplementary motor area during a delayed cued finger movement task was measured by time-resolved functional magnetic resonance imaging. Activity during movement preparation can be resolved from activity during movement execution in a single trial. All three areas were active during both movement preparation and movement execution. Activity in the primary motor cortex was considerably weaker during movement preparation than during movement execution; in the premotor cortex and the supplementary motor area, activity was of similar intensity during both periods. These observations are consistent with results from single neuronal recording studies in primates.

Quantitative relations between parietal activation and performance in mental rotation

The quantitative relationships between functional activation of the superior parietal lobule (SPL) and performance in the Shepard-Metzler mental rotation task were investigated in 16 human subjects using magnetic resonance (MR) imaging at high field (4 Tesla). Subjects were shown pairs of perspective drawings of three-dimensional objects and asked to judge whether they were the same or mirror images. Increased SPL activation was associated with a higher proportion of errors in performance. The increase in errors, and the concomitant increase in SPL activation, could be due to an increased difficulty in, and therefore increased demands for, information processing at several stages involved in making a decision, including encoding of the visual images shown, mentally rotating them, and judging whether they are the same or mirror images.

Interruption of motor cortical discharge subserving aimed arm movements

SummaryCan evolving motor commands be interrupted by changes in sensory signals that triggered them? We investigated this problem by observing the changes in single cell activity in the motor cortex of monkeys, changes that preceded movement of the hand toward a visual target. We found that this activity was interrupted following a shift of the target during the reaction or movement time and replaced by the pattern activity related to the movement towards the new target. This suggests that motor cortical commands subserving aimed arm movements are processes that can be interrupted in the course of their formation and/or execution by changes in afferent controlling inputs.

Three-dimensional drawings in isometric conditions: relation between geometry and kinematics

SummaryNormal human subjects grasped a 3-D isometric handle with an otherwise unrestrained, pronated hand and exerted forces continuously to draw circles, ellipses and lemniscates (figure-eights) in specified planes in the presence or absence of a 3-D visual force-feedback cursor and a visual template. Under any of these conditions and in all subjects, a significant positive correlation was observed between the instantaneous curvature and angular velocity, and between the instantaneous radius of curvature and tangential velocity; that is, when the force trajectory was most curved, the tangential velocity was lowest. This finding is similar to that obtained by Viviani and Terzuolo (1982) for 2-D drawing arm movements and supports the notion that central constraints give rise to the relation between geometric and kinematic parameters of the trajectory.

Manual interception of moving targets. II. On-line control of overlapping submovements

Abstractu2002We studied the kinematic characteristics of arm movements and their relation to a stimulus moving with a wide range of velocity and acceleration. The target traveled at constant acceleration, constant deceleration, or constant velocity for 0.5–2.0 s, until it arrived at a location where it was required to be intercepted. For fast moving targets, subjects produced single movements with symmetrical, bell-shaped velocity profiles. In contrast, for slowly moving targets, hand velocity profiles displayed multiple peaks, which suggests a control mechanism that produces a series of discrete submovements according to characteristics of target motion. To analyze how temporal and spatial aspects of these submovements are influenced by target motion, we decomposed the vertical hand velocity profiles into bell-shaped velocity pulses according to the minimum-jerk model. The number of submovements was roughly proportional to the movement time, resulting in a relatively constant submovement frequency (∼2.5 Hz). On the other hand, the submovement onset asynchrony showed significantly more variability than the intersubmovement interval, indicating that the submovement onset was delayed more following a submovement with a longer duration. Examination of submovement amplitude and its relation to target motion revealed that the subjects achieved interception mainly by producing a series of submovements that would keep the displacement of the hand proportional to the first-order estimate of target position at the end of each submovement along the axis of hand movement. Finally, we did not find any evidence that information regarding target acceleration is properly utilized in the production of submovements.