Motor cortical activity preceding a memorized movement trajectory with an orthogonal bend

Two monkeys were trained to make an arm movement with an orthogonal bend, first up and then to the left (), following a waiting period. They held a two-dimensional manipulandum over a spot of light at the center of a planar working surface. When this light went off, the animals were required to hold the manipulandum there for 600–700 ms and then move the handle up and to the left to receive a liquid reward. There were no external signals concerning the go time or the trajectory of the movement. It was hypothesized that during that period signs of directional processing relating to the upcoming movement would be identified in the motor cortex. Following 20 trials of the memorized movement trajectory, 40 trials of visually triggered movements in radially arranged directions were performed. The activity of 137 single cells in the motor cortex was recorded extracellularly during performance of the task. It was found that 62.8% of the cells changed activity during the memorized waiting period. During the waiting period, the population vector (Georgopoulos et al. 1983, 1984) began to grow approximately 130 ms after the center light was turned off; it pointed first in the direction of the second part of the memorized movement () and then rotated clockwise towards the direction of the initial part of the movement (). These findings indicate processing of directional information during the waiting period preceding the memorized movement. This conclusion was supported by the results of experiments in ten human subjects, who performed the same memorized movement (). In 10% of the trials a visual stimulus was shown in radially arranged directions in which the subjects had to move; this stimulus was shown at 0, 200, and 400 ms from the time the center light was turned off. We found that as the interval increased the reaction time shortened for the visual stimulus that was in the same direction as the upward component of the memorized movement.     

Shift of preferred directions of premotor cortical cells with arm movements performed across the workspace

Summary The activity of 156 neurons was recorded in the premotor cortex (Weinrich and Wise 1982) and in an adjoining rostral region of area 6 (area 6 DR; Barbas and Pandya 1987) while monkeys made visually-guided arm movements of similar direction within different parts of space. The activity of individual neurons varied most for a given preferred direction of movement within each part of space. These neurons (152/156, 97.4%) were labeled as directional. The spatial orientation of their preferred directions shifted in space to follow the rotation of the shoulder joint necessary to bring the arm into the different parts of the work-space. These results suggest that the cortical areas studied represent arm movement direction within a coordinate system rotating with the arm and where signals about the movement direction relate to the motor plan through a simple invariant relationship, that between cell preferred direction and arm orientation in space.     

Cognitive spatial-motor processes

Summary We studied the activity of 123 cells in the arm area of the motor cortex of three rhesus monkeys while the animals performed a 2-dimensional (2-D) step-tracking task with or without a delay interposed between a directional cue and a movement triggering signal. Movements of equal amplitude were made in eight directions on a planar working surface, from a central point to targets located equidistantly on a circle. The appearance of the target served as the cue, and its dimming, after a variable period of time (0.5–3.2 s), as the go stimulus to trigger the movement to the target; in a separate task, the target light appeared dim and the monkey moved its hand towards it without waiting. Population histograms were constructed for each direction after the spike trains of single trials were aligned to the onset of the cue. A significant increase (3–4×) in the population activity was observed 80–120 ms following the cue onset; since the minimum delay was 500 ms and the average reaction time approximately 300 ms, this increase in population activity occurred at least 680–720 ms before the onset of movement. A directional analysis (Georgopoulos et al. 1983, 1984) of the changes in population activity revealed that the population vector during the delay period pointed in the direction of movement that was to be made later.     

Cognitive spatial-motor processes

Summary Two rhesus monkeys were trained to move a handle on a two-dimensional (2-D) working surface either towards a visual stimulus (direct task) or in a direction orthogonal and counterclockwise (CCW) from the stimulus (transformation task), depending on whether the stimulus appeared dim or bright, respectively. Thus the direction of the stimulus (S, in polar coordinates) and the direction of the movement (M) were the same in the direct task but differed in the transformation task, such that M = S + 90°CCW. The task (i.e. brightness) condition (k = 2, i.e. direct or transformation) and the direction of the stimulus (m = 8, i.e. 8 equally spaced directions on a circle) resulted in 16 combinations (k × m = 16 classes) that were varied from trial to trial in a randomized block design. In 8 of these combinations the direction of the stimulus was the same for both tasks, whereas the direction of the movement was the same in the remaining 8 cases.The electrical signs of cell activity (N = 394 cells) in the arm area of the motor cortex (contralateral to the performing arm) were recorded extracellularly. The neural activity was analyzed at the single cell and neuronal population levels, and a modeling of the time course of single activity during the transformation task was carried out. We found the following, (a) Individual cells were active in both tasks; no cells were found that were active exclusively in only one of the two tasks. The patterns of single cell activity in the transformation task frequently differed from those observed in the direct task when the stimulus or the movement were the same. More specifically, cells could not be consistently classified as movement-or stimulus-related for frequently the activity of a particular cell would seem movement-related for a particular stimulus-movement combination, stimulus-related for another combination, or unrelated to either movement or stimulus for still another combination. Thus no real insight could be gained from such an analysis of single cell activity. (e) In a different analysis, we explored the idea that a changing directional signal could be detected in the time course of single cell activity during the reaction time. For that purpose we modeled the time course of single activity observed in the transformation task as a linear, weighted combination of influences from the direct task, taking the time patterns of cell activity during the stimulus, intermediate and movement directions in the direct task as estimates of the postulated directional influences. The results were inconclusive, in the sense that the best weighting scheme led to more than 46 % error in prediction in more than 50 % of the comparisons. Moreover, various combinations gave closely similar predictions. (c) An analysis of the activity of the neuronal population using the time evolution of the neuronal population vector (Georgopoulos et al. 1984) revealed an orderly rotation of the neuronal population vector from the direction of the stimulus towards the direction of the movement through the 90°CCW angle. (d) The hypothesis was tested that this apparent rotation of the population vector could be the result of activation of two subsets of cells, one with preferred directions at or near the stimulus direction, and the other with preferred directions at or near the movement directions: if cells of the former type were recruited at the beginning of the reaction time, followed by those of the second type, then the vector sum of the two could provide the rotating population vector. However, such a preferential activation of stimulus-direction centered and movement-direction centered cells was not observed. (e) On the other hand, a true rotation of the population vector could be reflected in the engagement of cells with intermediate preferred directions during the middle of the reaction time. Indeed, such a transient increase in the recruitment of cells with intermediate (i.e. between the stimulus and movement) preferred directions during the middle of the reaction time was observed. This supports the idea of a true rotation of the population signal.     

Differential relation of discharge in primary motor cortex and premotor cortex to movements versus actively maintained postures during a reaching task

The activity of cells in primary motor cortex (MI) and dorsal premotor cortex (PMd) were compared during reaching movements in a reaction-time (RT) task, without prior instructions, which required precise control of limb posture before and after movement. MI neurons typically showed strong, directionally tuned activity prior to and during movement as well as large gradations of tonic activity while holding the limb over different targets. The directionality of their movementand posture-related activity was generally similar. Proximal-arm muscles behaved similarly. This is consistent with a role for MI in the moment-to-moment control of motor output, including both movement and actively maintained postures, and suggests a common functional relation for MI cells to both aspects of motor behavior. In contrast, PMd cells were generally more phasic, frequently emitting only strong bursts of activity confined mainly to the behavioral reaction time before movement onset. PMd tonic activity during different postures was generally weaker than in MI, and showed a much more variable relation with their movement-related directional tuning. These results imply that the major contribution of PMd to this RT task occurred prior to the onset of movement itself, consistent with a role for PMd in the selection and planning of visually guided movements. Furthermore, the nature of the relative contribution of PMd to movement versus actively maintained postures appears to be fundamentally different from that in MI. Finally, there was a continuous gradient of changes in responses across the rostrocaudal extent of the precentral gyrus, with no abrupt transition in response properties between PMd and MI.     

Effects of hand movement path on motor cortical activity in awake,behaving rhesus monkeys

Summary Neuronal activity was studied in the primary (M1), supplementary (M2), dorsal premotor (PMd), and ventral premotor (PMv) cortex of awake, behaving rhesus monkeys. The animals performed forelimb movements to three targets, each approached by three different types of trajectories. With one trajectory type, the monkey moved its hand straight to the target, with another, the path curved in a clockwise direction, and with a third, the path curved in a counter-clockwise direction. We examined whether neuronal activity in these areas exclusively reflects a hand movement's net distance and direction or, alternatively, whether other factors also influence cortical activity. It was found that neuronal activity during all phases of a trial reflects aspects of movement in addition to target location. Among these aspects may be selection of an integrated motor act from memory, perhaps specifying the entirety of a path by which the hand moves to a target.     

Motor cortical modulation of the macaque red nucleus

Summary The nuclei of the neocerebellum receive inputs from somatosensory receptors and the motor cortex. In cats, the discharge of those nuclear neurons which were driven by passive movement of a limb segment in one direction was suppressed by stimulation of the cortical site from which movement was evoked in the opposite direction (Larsen and Yumiya 1979a). The cortical-evoked suppression of cerebellar neurons resulted in a disfacilitation of red nucleus neurons whose discharge elicited movement in the same direction as the cortical neurons from which the suppression was evoked and which were driven by passive movement in the opposite direction (Larsen and Yumiya 1980a). The purpose of this study was to determine if the cortical modulation of rubral neurons is organized in macaque monkeys in the same way as it is in cats. Red nucleus neurons were characterized by their response to natural stimulation of somatosensory receptors, and their response to cortical microstimulation was examined in peristimulus time histograms (PSTHs). Cortical stimulation evoked a short-latency corticorubral facilitation and a longer latency response which was presumed to be mediated by the cerebellum and which was composed primarily of suppression but was sometimes preceded by a brief facilitation. As was true in cats, over half of the rubral neurons which were driven by passive movement of a limb segment in one direction responded with a facilitation-suppression to stimulation of the agonistic cortical site from which movement was evoked in the opposite direction, but only a few responded to stimulation of the antagonistic cortical sites. Similar responses were evoked in many rubral neurons by stimulation of other cortical sites from which movement was elicited about the same joint in a different plane or at a joint adjacent to that whose passive movement drove the rubral neuron. Responses were found in neurons which received somatosensory input from proximal or distal limb segments and in neurons in the parvocellular or magnocellular divisions of the nucleus, although the corticorubral facilitation was found more frequently in parvocellular neurons. In conclusion, the motor cortical modulation of the red nucleus and cerebellum is similar in monkeys and cats, and is the same for the proximal and distal limb representation.This research was supported in part by NIH grant NS10705     

Motor preparation in a memorised delay task

The effect on reaction time (RT) and movement time (MT) of remembering which one of several targets to move to was investigated in 18 participants who completed 416 trials in each task. On each trial, participants moved their index finger from a central, illuminated switch (the stimulus) to one of eight targets located on the circumference of a 6 cm radius circle. A visual cue (illumination of the target) informed the participant of the appropriate target. In the memorised delay task, the cued target was lit for 300 ms followed by a variable (450–750 ms) foreperiod during which the participant was required to remember the location of the target until the stimulus light was extinguished. In the non-memorised delay task, the target remained lit during the entire foreperiod (750–1050 ms) until the response was completed. At the go signal (stimulus light extinguished) participants moved as quickly and accurately as possible to the cued target. Both RT and MT were significantly (p<0.05) longer in the memorised delay task. The increase in RT shows that remembering which target imposed a greater load on motor preparation even though all the information needed for preparing the response was presented in the cue at the beginning of each trial. The increase in MT raises the possibility that movement execution was also programmed during motor preparation.     

Hypothetical joint-related coordinate systems in which populations of motor cortical neurons code direction of voluntary arm movements

Results of the recent electrophysiological experiments by Caminiti et al. suggest that populations of neurons of the motor areas code direction of voluntary arm movement in an intrinsic coordinate system. In this letter I propose a set of joint-related coordinate systems that rotate with the posture of the arm in which populations of motor cortical neurons code direction of the arm movement. In these frames of reference, the movement directions represented vary with the posture of the arm but the preferred directions of the motor cortical neurons do not rotate. It is suggested that the difference in the neuronal activity for different workspaces, which was observed by Caminiti et al., is due to the dependence of the movement direction, represented in one of the joint-related coordinate systems, on the posture of the arm.     

ERP correlates of linear hand movements in a motor reproduction task

Blindfolded participants performed one‐dimensional movements towards a mechanical stop and back to the start. After a varying delay, they had to reproduce the encoded target position by a second mechanically unrestricted movement. Average event‐related potentials accompanying the “encoding” and the “reproduction” movements revealed a biphasic waveshape over primary sensorimotor areas. The first negative deflection was the gradually increasing motor potential (MP) that precedes movement onset. This was followed by a second negative component (N4) starting about 100 ms after movement onset. Its amplitude and latency increased with increasing movement distance and reached its maximum in unrestricted movements (i.e., during reproduction) shortly before the deceleration peak. These results show that rapid hand movements are accompanied by non‐continuous and highly distance specific activity changes measured over the sensorimotor cortex.     

Motor adaptation to a small force field superimposed on a large background force

The human motor system adapts to novel force field perturbations during reaching by forming an internal model of the external dynamics and by modulating arm impedance. We studied whether it uses similar strategies when the perturbation is superimposed on a much larger background force. Consistent with the Weber–Fechner law for force perception, subjects had greater difficulty consciously perceiving the force field perturbation when it was superimposed on the large background force. However, they still adapted to the perturbation, decreasing trajectory distortion with repeated reaching and demonstrating kinematic after effects when the perturbation was unexpectedly removed. They also adapted by increasing their arm impedance when the background force was not present, but did not vary the arm impedance when the background force was present. The identified parameters of a previously proposed mathematical model of motor adaptation changed significantly with the presence of the background force. These results indicate that the motor system maintains its sensitivity for internal model formation even when there are large background forces that mask perception. Further, the motor system modulates arm impedance differently in response to the same perturbation depending on the background force onto which that perturbation is superimposed. Finally, these results suggest that computational models of motor adaptation will likely need to include force-dependent parameters to accurately predict errors.     

Performance of a motor task after cerebellar cortical lesions in rats

Rats with lesions of the cerebellar cortex of the hemispheres, the lobus medius of the vermis and the caudal vermis were tested on a difficult motor task. Hemisphere lesions produced no significant deficits but lesions of the medial and caudal vermis did. No evidence of recovery was seen in the latter two groups.     

An output zone of the monkey primary motor cortex specialized for bilateral hand movement

Summary We have identified a subregion in the monkey primary precentral motor cortex (MI) that is characterized by its relationship to bilateral or ipsilateral hand movements. The subregion is located between the digit and face representation areas. The majority of single cells in this portion of MI exhibit distinct activity before and during visually triggered key-press movements performed by means of ipsilateral or contralateral digit flexion. Intracortical microstimulation evoked responses of ipsilateral, in addition to contralateral, digit muscles.     

Changes of slow cortical negative DC-potentials during the acquisition of a complex finger motor task

Summary To study whether electrophysiological correlates of increasing motor skill can be demonstrated in man, we recorded cortical negative DC-potentials during the acquisition of a complex finger movement in 21 subjects. The movement consisted in moving a matchstick to and fro between the index finger (II) and the little finger (V). Cortical negative DC-potentials were recorded at Fz, Cz, C1, C2 and Pz. As a control a simple finger movement was performed during the same session by 7 of the Ss. Both tasks were repeated 60–80 times and averages of the first and the last 15 artifact-free single runs were compared. Whereas only a slight, inconstant decrease in surface electronegativity during the simple motor task was observed, a significant reduction in potential size occurred during the complex task at Cz (maximum), C1, C2 and Pz but not at Fz. In addition, a significant difference in the decrease of surface electronegativity between various electrode positions was observed. We suggest that these changes in potential size during the process of motor learning may reflect an altered cortical organisation of movement control during the acquisition of a complex motor task.This article is dedicated to the memory of the late Professor Dr. Richard Jung who encouraged and initiated these investigations     

Learning and recall of incremental kinematic and dynamic sensorimotor transformations

Numerous studies have shown that when people encounter a sudden and novel sensorimotor transformation that alters perceived or actual movement, they gradually adapt and can later recall what they have learned if they encounter the transformation again. In this study, we tested whether retention and recall of learning is also observed when kinematic and dynamic transformations are introduced incrementally such that participants never experience large movement errors. Participants adapted their reaching movements to either a visuomotor rotation of hand position (kinematic transformation) or a rotary viscous force-field applied to the hand (dynamic transformation). These perturbations were introduced either incrementally or instantaneously. Thus, four groups of participants were tested with an incremental and an instantaneous group for both the kinematic and dynamic perturbations. To evaluate retention of learning, participants from all four groups were tested a day later on the same kinematic or dynamic perturbation presented instantaneously (at full strength). As expected, we found that subjects in the instantaneous group retained learning across days. We also found that, for both kinematic and dynamic perturbations, retention was equally good or better when the transformation was introduced incrementally. Because large and clearly detectable movement errors were not observed during adaptation to incremental perturbations, we conclude that such errors are not required for the learning and retention of internal models of kinematic and dynamic sensorimotor transformations.     

Neuronal activity related to eye-hand coordination in the primate premotor cortex

To test the functional implications of gaze signals that we previously reported in the dorsal premotor cortex (PMd), we trained two rhesus monkeys to point to visual targets presented on a touch screen while controlling their gaze orientation. Each monkey had to perform four different tasks. To initiate a trial, the monkey had to put his hand on a starting position at the center of the touch screen and fixate a fixation point. In one task, the animal had to make a reaching movement to a peripheral target randomly presented at one of eight possible locations on a circle while maintaining fixation at the center of this virtual circle (central fixation + reaching). In the second task, the monkey maintained fixation at the location of the upcoming peripheral target and, later, reached to that location. After a delay, the target was turned on and the monkey made a reaching arm movement (target fixation + reaching). In the third task, the monkey made a saccade to the target without any arm movement (saccade). Finally, in the fourth task, the monkey first made a saccade to the target, then reached to it after a delay (saccade + reaching). This design allowed us to examine the contribution of the oculomotor context to arm-related neuronal activity in PMd. We analyzed the effects of the task type on neuronal activity and found that many cells showed a task effect during the signal (26/60; 43%), set (16/49; 33%) and/or movement (15/54; 28%) epochs, depending on the oculomotor history. These findings, together with previously published data, suggest that PMd codes limb-movement direction in a gaze-dependent manner and may, thus, play an important role in the brain mechanisms of eye-hand coordination during visually guided reaching. Received: 10 September 1998 / Accepted: 19 March 1999     

Neuronal activity of somatosensory cortex in a cross-modal (visuo-haptic) memory task

Studies have shown that in the monkey′s associative cerebral cortex, cells undergo sustained activation of discharge while the animal retains information for a subsequent action. Recent work has revealed the presence of such ″memory cells″ in the anterior parietal cortex (Brodmann′s areas 3a, 3b, 1, and 2) – the early stage of the cortical somatosensory system. Here we inferred that, in a cross-modal visuo-haptic short-term memory task, somatosensory cells would react to visual stimuli associated with tactile features. Single-unit discharge was recorded from the anterior parietal cortex – including areas of hand representation – of monkeys performing a visuo-haptic delayed matching-to-sample task. Units changed firing frequency during the presentation of a visual cue that the animal had to remember for making a correct tactile choice between two objects at the end of a delay (retention period). Some units showed sustained activation during the delay. In some of them that activation differed depending on the cue. These findings suggest that units in somatosensory cortex react to visual stimuli behaviorally associated with tactile information. Further, the results suggest that some of these neurons are involved in short-term active memory and may, therefore, be part of cross-modal memory networks. Received: 24 March 1997 / Accepted: 8 May 1997     

Precentral unit activity related to control of arm movements

Summary 1. Precentral neural activity was studied in relation to steady loads in a Cebus monkey trained to make self-paced elbow flexions and extensions into learned target positions in which the arm had to be held steady between movements. The same steady loads were applied in about 15 successive trials. 2. Single unit records were analyzed from 75 task-related precentral cortical cells. Out of 57 activated neurons, 18 reached peak discharge before or at movement onset, 31 after movement onset, and 8 had gradually rising discharge throughout holding and movement. 3. Different steady loads were tested adequately for 52 neurons. Of these 13 displayed a clear increase of the static discharge rate during the hold phase; a weak trend in the same direction was seen in additional 11 neurons. Four neurons appeared to be related to position rather than to load, and 24 neurons did not change their static discharge rate under different loads. 4. Increasing load produced also dynamic changes of firing frequency in 8 neurons: an increase of the peak frequency, a shortening of the rise time to peak, and advanced onset time. Increased peak frequency was positively correlated with increased peak acceleration of the movement. 5. It is likely that these dynamic changes occurring before or shortly after movement onset are programmed and not the consequence of proprioceptive feedback.Supported in part by the Medical Research Council of Canada (MT-4465) and the U. S. Public Health Servic (NS-10311)     

Motor memory preservation in aged monkeys mirrors that of aged humans on a similar task

We studied long-term motor memory preservation in rhesus monkeys tested on a task similar to that employed in humans. First, motor speed and rate of motor decline was measured in 23 animals ranging from 4 to 26 years old. The task for the animals consisted of removing a food reward from a curved rod within the inner chamber of an automated panel. Young animals performed twice as fast as the aged animals. Second, young (n = 6) and aged (n = 10) animals were re-tested 1 year later on the same task with no intervening practice. We anticipated a decline in motor speed of 144 ms/year, instead the average performance time recorded during the repeat session improved significantly by 17% in the aged animals. This finding mirrors that of a longitudinal study conducted in humans using a similar test panel and supports that, while initial performance times of a novel motor task decline with age, motor memory traces are preserved over an extended time interval, even without continued practice. The data also support that the rhesus monkey could be used as a model to study the mechanisms by which long-term retention of motor memory occurs in aging.