John F. Kalaska

Neural Mechanisms for Interacting with a World Full of Action Choices

The neural bases of behavior are often discussed in terms of perceptual, cognitive, and motor stages, defined within an information processing framework that was originally inspired by models of human abstract problem solving. Here, we review a growing body of neurophysiological data that is difficult to reconcile with this influential theoretical perspective. As an alternative foundation for interpreting neural data, we consider frameworks borrowed from ethology, which emphasize the kinds of real-time interactive behaviors that animals have engaged in for millions of years. In particular, we discuss an ethologically-inspired view of interactive behavior as simultaneous processes that specify potential motor actions and select between them. We review how recent neurophysiological data from diverse cortical and subcortical regions appear more compatible with this parallel view than with the classical view of serial information processing stages.

Neural Correlates of Reaching Decisions in Dorsal Premotor Cortex: Specification of Multiple Direction Choices and Final Selection of Action

We show that while a primate chooses between two reaching actions, its motor system first represents both options and later reflects selection between them. When two potential targets appeared, many (43%) task-related, directionally tuned cells in dorsal premotor cortex (PMd) discharged if one of the targets was near their preferred direction. At the population level, this generated two simultaneous sustained directional signals corresponding to the current reach options. After a subsequent nonspatial cue identified the correct target, the corresponding directional signal increased, and the signal for the rejected target was suppressed. The PMd population reliably predicted the monkeys response choice, including errors. This supports a planning model in which multiple reach options are initially specified and then gradually eliminated in a competition for overt execution, as more information accumulates.

Parietal area 5 neuronal activity encodes movement kinematics, not movement dynamics

SummaryA previous study reported that proximal-arm related area 5 neurons showed continuously-graded changes in activity during unloaded arm movements in different directions (Kalaska et al. 1983), which resembled the responses of primary motor cortex cells in several respects (Georgopoulos et al. 1982). We report here that loading the arm reveals an important difference between cell activity in the two areas. Loads were continuously applied to the arm in different directions. The loads produced large continuously-graded changes in muscle activity but did not alter the handpath or joint angle changes of the arm during the movements. The activity of most area 5 cells was only weakly affected by the loads, and the overall pattern of population activity was virtually unaltered under all load conditions. This indicates that area 5 activity encodes the invariant spatial parameters (kinematics) of the movements. In contrast, many motor cortex cells showed large changes in activity during loading, and so signal the changing forces, torques or muscle activity (movement dynamics; Kalaska et al. 1989).

Neural correlates of mental rehearsal in dorsal premotor cortex

Behavioural and imaging studies suggest that when humans mentally rehearse a familiar action they execute some of the same neural operations used during overt motor performance. Similarly, neural activation is present during action observation in many of the same brain regions normally used for performance, including premotor cortex. Here we present behavioural evidence that monkeys also engage in mental rehearsal during the observation of sensory events associated with a well-learned motor task. Furthermore, most task-related neurons in dorsal premotor cortex exhibit the same activity patterns during observation as during performance, even during an instructed-delay period before any actual observed motion. This activity might be a single-neuron correlate of covert mental rehearsal.

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.

Comparison of variability of initial kinematics and endpoints of reaching movements

Abstract The accuracy of reaching movements to memorized visual target locations is presumed to be determined largely by central planning processes before movement onset. If so, then the initial kinematics of a pointing movement should predict its endpoint. Our study examined this hypothesis by testing the correlation between peak acceleration, peak velocity, and movement amplitude and the correspondence between the respective spatial positions of these kinematic landmarks. Subjects made planar horizontal reaching movements to targets located at five different distances and along five radially arrayed directions without visual feedback during the movements.The spatial dispersion of the positions of peak acceleration, peak velocity, and endpoint all tended to form ellipses oriented along the movement trajectory. However, whereas the peaks of acceleration and velocity scaled strongly with movement amplitude for all of the movements made at the five target distances in any one direction, the correlations with movement amplitude were more modest for trajectories aimed at each target separately. Furthermore, the spatial variability in direction and extent of the distribution of positions of peak acceleration and peak velocity did not scale differently with target distance, whereas they did for endpoint distributions. Therefore, certain features of the final kinematics are evident in the early kinematics of the movements as predicted by the hypothesis that they reflect planning processes. However, endpoint distributions were not completely predetermined by the Initial kinematics. In contrast, multivariate analysis suggests that adjustments to movement duration help compensate for the variability of the initial kinematics to achieve desired movement amplitude. These compensatory adjustments do not contradict the general conclusion that the systematic patterns in the spatial variability observed in this study reflect planning processes. On the contrary, and consistent with that conclusion, our results provide further evidence that direction and extent of reaching movements are planned and determined in parallel over time.

Neuronal activity in primate parietal cortex area 5 varies with intended movement direction during an instructed-delay period

SummaryA monkey was trained to make arm movements to visual targets immediately after presentation of a GO signal, either in a visual reaction-time paradigm (CONTROL task), or after an instructed-delay period of variable duration, during which a CUE stimulus signalled the direction of the impending movement (DELAY task). The activity of 98 area 5 cells recorded in 2 hemispheres varied with movement direction in the CONTROL task. This included 60 “early” cells which showed directional activity changes prior to movement onset. In the DELAY task, 54/98 cells (55%) showed activity changes during the instructed-delay period which varied with the direction of the impending movement. Most of these (45/54, 83%) were “early” cells. Forty proximal arm-related cells were recorded in adjacent area 2. In contrast to area 5, only 2/40 area 2 cells showed any evidence of changes in activity varying with intended movement direction during the instructed-delay period. The origin of area 5 activity changes during an instructed-delay period which are related to intended direction of a delayed movement is uncertain, but its presence is consistent with a number of proposed roles for area 5.

Differential effect of task conditions on errors of direction and extent of reaching movements

Abstract Invariant patterns in the distribution of the endpoints of reaching movements have been used to suggest that two important movement parameters of reaching movements, direction and extent, are planned by two independent processing channels. This study examined this hypothesis by testing the effect of task conditions on variable errors of direction and extent of reaching movements. Subjects made reaching movements to 25 target locations in a horizontal workspace, in two main task conditions. In task 1, subjects looked directly at the target location on the horizontal workspace before closing their eyes and pointing to it. In task 2, arm movements were made to the same target locations in the same horizontal workspace, but target location was displayed on a vertical screen in front of the subjects. For both tasks, variable errors of movement extent (on-axis error) were greater than for movement direction (off-axis error). As a result, the spatial distributions of endpoints about a given target usually formed an ellipse, with the principal axis oriented in the mean movement direction. Also, both on- and off-axis errors increased with movement amplitude. However, the magnitude of errors, especially on-axis errors, scaled differently with movement amplitude in the two task conditions. This suggests that variable errors of direction and extent can be modified independently by changing the nature of the sensorimotor transformations required to plan the movements. This finding is further evidence that the direction and extent of reaching movements appear to be controlled independently by the motor system.

Muscle synergies during locomotion in the cat: a model for motor cortex control

It is well established that the motor cortex makes an important contribution to the control of visually guided gait modifications, such as those required to step over an obstacle. However, it is less clear how the descending cortical signal interacts with the interneuronal networks in the spinal cord to ensure that precise changes in limb trajectory are appropriately incorporated into the base locomotor rhythm. Here we suggest that subpopulations of motor cortical neurones, active sequentially during the step cycle, may regulate the activity of small groups of synergistic muscles, likewise active sequentially throughout the step cycle. These synergies, identified by a novel associative cluster analysis, are defined by periods of muscle activity that are coextensive with respect to the onset and offset of the EMG activity. Moreover, the synergies are sparse and are frequently composed of muscles acting around more than one joint. During gait modifications, we suggest that subpopulations of motor cortical neurones may modify the magnitude and phase of the EMG activity of all muscles contained within a given synergy. Different limb trajectories would be produced by differentially modifying the activity in each synergy thus providing a flexible substrate for the control of intralimb coordination during locomotion.

Common codes for situated interaction

A common code for integrating perceptions and actions was relevant for simple behavioral guidance well before the evolution of cognitive abilities. We review proposals that representation of to-be-produced events played important roles in early behavior, and evidence that the neural mechanisms supporting such rudimentary sensory predictions have been elaborated through evolution to support the cognitive codes addressed