| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
|
|
|
|||||||
|
|||||||||
Department of Neurology, Emory University School of Medicine, Atlanta, Georgia 30322
 |
ABSTRACT |
|---|
 Abstract
 Introduction
Methods
Results
Discussion
References
|
|---|
Shen, Liming and Garrett E. Alexander. Preferential representation of instructed target location versus limb trajectory in dorsal premotor area. J. Neurophysiol. 77: 1195-1212, 1997. The dorsal premotor area (PMd) of monkeys has been implicated in processes relating to movement preparation and movement selection. In the present study, we sought to determine whether PMd neurons that are activated during a delayed reaching task have directional responses that reflect either the target (i.e., the goal) of an intended movement or the physical properties of the movement itself. Two macaque monkeys were trained to perform a visually instructed, delayed reaching task with indirect visual feedback. The subjects and methods were identical to those described in the preceding paper. In the behavioral task, each subject moved a two-dimensional joystick with the right forelimb to align a cursor with targets presented on a video display. The paradigm dissociated the direction of forelimb movement from the spatial location of the target. This was accomplished by varying the spatial mappings between joystick and cursor. A variable delay separated the visual stimulus that instructed the target location (IS) from the visual stimulus that triggered the instructed movement (TS). Task-related activity was recorded from a total of 181 PMd neurons. The focus of this study was on directionally tuned neuronal responses that included 1) stimulus-related activity (phasic, following IS); 2) set-related activity (tonic, between IS and TS); and 3) movement-related activity (phasic, following TS). Of the entire sample of PMd neurons with directionally tuned activity, 114 were tested with two joystick/cursor mappings, permitting dissociation of directional responses that depended on limb trajectory from those that depended on target location. Task-related neuronal activity was classified as target-dependent if it covaried exclusively with target location across both conditions, and as limb-dependent if it covaried exclusively with limb trajectory. Directional activity that changed significantly across rotation conditions was classified as complex. Approximately one half of the sample of PMd neurons showed stimulus-related activity that was directionally tuned (56%, 64 of 114). Nearly all of the directionally classifiable stimulus-related activity was target dependent (94%, 44 of 47 responses), and none was limb dependent. A small proportion was classified as complex (6%, 3 of 47 responses). More than two thirds of the PMd neurons showed set-related activity that was directionally tuned (69%, 79 of 114). Among cells with set-related activity that was directionally classifiable, there were ~9 times as many target-dependent responses (76%, 48 of 63) as there were limb-dependent responses (8%, 5 of 63), with the remainder being complex (16%, 10 of 63). Approximately three quarters of the sample of PMd neurons showed early movement-related activity (before movement onset) that was directionally tuned (78%, 89 of 114). Among those cells whose early movement-related activity was directionally classifiable, there were >3 times as many target-dependent responses (51%, 34 of 66) as limb-dependent responses (14%, 9 of 66), with the remainder being complex (35%, 23 of 66). Approximately two thirds of the sample showed late movement-related responses (after movement onset) that were directionally tuned (68%, 78 of 114). Among those cells whose late movement-related activity was directionally classifiable, there were comparable numbers of target-dependent (25%, 15 of 61) and limb-dependent responses (28%, 17 of 61), with the remainder being complex (47%, 29 of 61). These results indicate a preferential representation of target location rather than limb trajectory among PMd neurons. Over the extended interval from IS to motor response, there was a gradual decline in the frequency of target-dependent activity and corresponding increases in the frequencies of both limb-dependent and complex activity. These findings suggest that PMd neurons may participate in mediating the sensory-to-motor transformation required by the delayed reaching task. Comparison of the responses of PMd neurons with those of motor cortex neurons recorded in the same experimental subjects indicates that PMd may play a preferential role in sensory or context-dependent processing related to task performance, whereas motor cortex may be more involved in processing related to the purely motor aspects of task performance.
The dorsal premotor area (PMd) of monkeys has been implicated in processes relating to movement preparation and movement selection, particularly with respect to movements whose selection depends on the behavioral context (Boussaoud and Wise 1993a The subjects, behavioral paradigms, and experimental design, including data acquisition and data analysis procedures, were those described in the accompanying paper (Shen and Alexander 1997 Data base
A total of 181 PMd neurons (95 from monkey JA, 86 from monkey KO) showed some form of task-related activity, that is, activity that showed significant directional effects or that differed significantly from baseline levels during at least one of the task-defined epochs (including the pre-IS epoch). Only neurons whose task-related responses had been tested with both rotation conditions were included in the final data base, which comprised 114 cells.
Overview of task-related activity
For the sample as a whole, the most prominent task-related activity that we observed among PMd neurons was set related. The distribution and functional categorization of task-related activity across the various epochs that followed the IS are summarized in Table 1. Approximately four fifths of the neurons in the sample showed tonic, set-related activity during the postinstruction (delay) period. The majority of the stimulus-, set-, and movement-related responses were directional, that is, they showed significant dependence on the spatial features of the task. Approximately two thirds of the stimulus- and set-related responses that were directional were found to depend strictly on either the direction of limb movement or the location of the target. Nearly one half of the sample of PMd neurons showed tonic, nondirectional anticipatory activity preceding delivery of the visual IS, and a small proportion of neurons showed only this type of task-related activity.
Phasic, stimulus-related activity following the IS
Approximately three quarters of the sample of PMd neurons showed brief, phasic activity changes immediately following the IS (Table 1), and the majority of these responses were directionally tuned. Slightly more than one half of the entire sample showed stimulus-related activity that was directionally selective (56%, 64 of 114 responses). Of the stimulus-related activity that was directionally classifiable, nearly all was target-dependent (94%, 44 of 47 responses), and none was limb-dependent. A small proportion was classified as complex (6%, 3 of 47 responses). An example of stimulus-related activity that was classified as target-dependent is illustrated in Fig. 1. In both the nonrotated and the rotated conditions, this cell showed a phasic burst of activity that began shortly after presentation of the IS at either the right target or the bottom target, irrespective of the eventual direction of limb movement. There was no response when the IS was presented at either of the other two targets.
Tonic, set-related activity preceding the TS
Approximately four fifths of the entire sample of PMd neurons showed tonic, set-related activity during the postinstruction (delay) epoch between IS and TS (Table 1), and the majority of this activity was directionally selective. Approximately two thirds of the entire sample showed set-related activity that was directionally tuned (69%, 79 of 114 responses). Among cells with set-related activity that was directionally classifiable, there were ~9 times as many target-dependent responses (76%, 48 of 63) as there were limb-dependent responses (8%, 5 of 63), with the remainder being complex (16%, 10 of 63).
Anticipatory or pre-cue activity preceding the IS
Although this was not an intended focus of our study, in nearly one half of our sample of PMd neurons (48%, 55 of 114) we observed tonic increases in discharge rate during the interval between the monkey's capture of the center fixation point and onset of the IS (pre-IS epoch). Such activity, described previously by Wise and colleagues, was designated "anticipatory activity" by Mauritz and Wise (1986)
Phasic, movement-related activity following the TS
Movement-related activity following the TS was considered to be early or late, depending on whether it preceded or followed the onset of limb movement. Movement-related activity in PMd was generally monophasic, consisting of only a single component (either early or late, but not both). Approximately three quarters of the sample of PMd neurons showed early movement-related activity that was directionally tuned (Table 1). Of the early movement-related activity that was directionally classifiable, there were >3 times as many target-dependent responses (51%, 34 of 66) as limb-dependent responses (14%, 9 of 66), with the remainder being complex (35%, 23 of 66). Approximately two thirds of the sample of PMd neurons showed late movement-related activity that was directionally tuned (Table 1). Of the late movement-related activity that was directionally classifiable, there were comparable numbers of target-dependent (25%, 15 of 61) and limb-dependent responses (28%, 17 of 61), with the remainder being complex (47%, 29 of 61).
Complex activity
Some of the directional activity observed in this study (including stimulus-, set-, and movement-related responses) did not meet the criteria for classification as either target or limb dependent, because of complex interactions between direction and rotation condition. An example of complex set-related activity is illustrated in Fig. 10. In the 90° mapping condition, this cell showed a directional set-related response, with maximal discharge during the delay epoch that preceded leftward movements of the joystick to capture the bottom target. In the 0° mapping condition, however, the set-related response became nondirectional, consisting of sustained suppression of activity throughout the postinstruction period regardless of the designated target (or the instructed direction of limb movement). When this cell was again tested in the 90° mapping condition, the same directional set-related response was observed once more. This type of response might have been characterized, equivalently, as either a target- or a limb-dependent response whose directionality changed across rotation conditions. Because of this ambiguity, we have chosen to designate this type of response as complex.
Temporal distribution of directionally classifiable activity
Figure 11 shows the temporal distribution of target-dependent versus limb-dependent versus complex activity across the task-defined epochs that followed the IS onset. It is evident that, over the extended interval between IS and motor response, there was an initial predominance followed by a gradual decline in the proportion of PMd neurons showing target-dependent activity, and a gradual increase in the proportion of neurons showing limb-dependent activity. There was also a gradual increase in the proportion of neurons showing complex activity. An overall
Locations of neurons with task-related activity
Figure 12 shows the surface penetration sites for all microelectrode tracks that produced neuronal recordings that contributed to the final data base. The entire sample of PMd neurons with task-related responses was drawn from the immediate vicinity of the superior precentral sulcus. In each monkey, most of the task-related neurons were located in a region just ventral to the rostral half of the sulcus.
Comparison of neuronal responses in PMd with those
in MC
We compared, epoch by epoch, the relative frequencies of target- and limb-dependent responses observed in PMd with those observed in MC in the same experimental animals. The data from MC recordings were described in the preceding paper (Shen and Alexander 1997
One of the principal findings of this study was that the large majorities of directional stimulus-, set-, and early movement-related responses among PMd neurons proved to be target-dependent, showing selective dependence on the location of the target that guided the delayed reaching movement and not on the trajectory of the limb movement itself. The other main finding was that the relative frequencies of target-dependent, limb-dependent, and complex activity showed a systematic pattern of variation across the different task epochs between IS presentation and motor response.
Evidence for a sensory-to-motor transformation in PMd
To perform the instructed delay task that was used in this study, each monkey was required to transform the spatial information contained in the visual IS into a limb movement of appropriate trajectory. Over the sequence of epochs leading from IS onset to delayed motor response, we observed a gradual decline in the frequency of target-dependent activity and a gradual increase in the frequency of limb-dependent activity. This is consistent with the possibility that PMd may participate in mediating the sensory-to-motor transformation required by the task.
Comparison of recruitment patterns in PMd and MC
The fact that the PMd data described here and the MC data described in the accompanying paper (Shen and Alexander 1997 Sensory versus associative versus motor activity in PMd
In the preceding paper (Shen and Alexander 1997 Interpretational limitations
We have already considered the main interpretational limitations of our experimentatal design in the accompanying paper (Shen and Alexander 1997 Cortical networks for spatial sensory-to-motor transformations
The evidence reviewed above suggests a general model of how the distributed network of cortical motor fields may participate in the planning and execution of visually instructed limb movements. The studies described in this and the accompanying paper (Shen and Alexander 1997
INTRODUCTION
Abstract
Introduction
Methods
Results
Discussion
References
,b; Crammond and Kalaska 1994; diPellegrino and Wise 1993b; Kurata and Hoffman 1994; Kurata and Tanji 1986; Kurata and Wise 1988; Mauritz and Wise 1986; Mushiake et al. 1991; Passingham 1988; Riehle and Requin 1989; Weinrich and Wise 1982; Weinrich et al. 1984; Wise and Mauritz 1985). Injections of muscimol into the PMd of monkeys resulted in increased numbers of directional errors during performance of a visually instructed, conditional forelimb movement task (Kurata and Hoffman 1994). Injections of bicuculline into PMd led to irrepressible reaching movements that were comparable with those that subjects had been trained to make in a delayed, visually instructed reaching task (Sawaguchi et al. 1996). Many PMd neurons show selective activation during an enforced delay when a movement-instructing stimulus (IS) has been delivered just before the delay begins. When directional, such delay- or set-related neuronal activity in PMd has generally been found to covary mainly with the trajectory of the instructed limb movement, rather than with any sensory features (i.e., physical properties) of the IS (Boussaoud and Wise 1993b; Crammond and Kalaska 1994; diPellegrino and Wise 1993b; Kurata and Wise 1988; Weinrich and Wise 1982; Weinrich et al. 1984). Similarly, movement-related activity in PMd has generally been found to covary with the trajectory of limb movement rather than with any sensory features of the IS (Boussaoud and Wise 1993b; Weinrich and Wise 1982; Weinrich et al. 1984). On the other hand, many PMd neurons also show transient responses to the IS itself, and much of this activity has been found to covary with specific properties of the sensory stimulus (such as its spatial location) rather than with the trajectory or other features of the resulting limb movement (Boussaoud and Wise 1993b; Crammond and Kalaska 1994; diPellegrino and Wise 1993b).
; Crammond and Kalaska 1994; diPellegrino and Wise 1993b; Kurata 1993; Weinrich and Wise 1982; Weinrich et al. 1984; Wise and Mauritz 1983, 1985). However, in one recent study monkeys were trained to reach along three different trajectories to capture the same target, and there it was found that some PMd neurons did show either stimulus-, set-, or movement-related activity that covaried with target location irrespective of the trajectory of limb movement (Hocherman and Wise 1991).
). Some of these results have been presented elsewhere in abstract form (Alexander and Shen 1995; Shen and Alexander 1995).
METHODS
Abstract
Introduction
Methods
Results
Discussion
References
), which focused exclusively on data obtained from MC. The data described in this report were obtained from single-cell recordings in PMd. The following is a brief summary of the methods.
= 0.001) were used to determine whether epoch-specific responses showed directional dependencies on the location of the target or on the trajectory of the instructed limb movement. The categories of spatial dependencies for neurons with directional responses included target-dependent (covarying selectively with the location of the target across both rotation conditions); limb-dependent (covarying selectively with the initial direction of limb movement across both rotation conditions); complex (directional, but not fulfilling the criteria for either target or limb dependence because of significant differences in spatial tuning across rotation conditions); and unclassifiable (fulfilling the criteria for both target and limb dependence).
RESULTS
Abstract
Introduction
Methods
Results
Discussion
References
View this table:
TABLE 1.
Categorization of task-related neuronal activity
in PMd
View larger version (29K):
[in a new window]
FIG. 1.
Target-dependent, stimulus-related activity recorded from a dorsal premotor area (PMd) neuron. Each of the 4 rows of illustrations represents the neural and kinematic data obtained from trials in which the same peripheral target served as the locus for the visual movement-instructing stimulus (IS, cue). Data from both 0° and 90° mapping conditions are presented. In this and subsequent figures that illustrate neuronal responses, data from the 2 rotation conditions are ordered from left (A) to right (B) in the sequence in which they were administered. The neural data are shown as corresponding raster displays (top) and perievent histograms (bottom). Each dot in the raster displays represents a single action potential, and each line of dots contains the data from a single trial. The time base (ms) is the same for rasters and histograms, both of which are aligned on the same behavioral event. The alignment point for the rasters is indicated by a single caret mark at the bottom of each raster display. Binwidth for histograms: 25 ms. Units for vertical scale: spikes/s. Trials are aligned with cue onset. The kinematic data are shown to the right of each corresponding set of neural data. The target-capturing hand trajectories from trials of a given type are superimposed and presented on a facsimile of the monkey's behavioral display, with the designated target for each trial type indicated by shading. Trajectories indicated as upward in the illustration represent forward limb movements, whereas those indicated as downward represent backward limb movements. The units for the horizontal scale under each kinematic display represent hand displacement (cm). This neuron responded to the presentation of the instructional cue with a brisk, phasic discharge whenever the visual IS was located at either the right or the bottom target, irrespective of rotation condition or movement trajectory. Although movements to the right target in the 0° mapping condition were not fully adapted (i.e., the initial direction of movement was more appropriate for the 90° mapping condition), the lack of stimulus-related activity preceding the fully adapted leftward movements to the left target in the 0° mapping condition confirms that this cell's stimulus-related activity depended on target location rather than the direction of limb movement.
View larger version (32K):
[in a new window]
FIG. 2.
Target-dependent set-related activity in PMd. Conventions are similar to those in Fig. 1, except that for each rotation condition there are 2 columns of rasters and histograms aligned, respectively, with the onsets of IS (cue) and movement-triggering stimulus (TS, trigger). Heavy dots in the trigger-aligned rasters: times of movement onset after delivery of the TS. Under both rotation conditions, this cell showed a tonic, set-related discharge throughout the postinstruction (delay) epoch between IS and TS on trials in which the bottom target had been designated as the correct target by the IS.
View larger version (54K):
[in a new window]
FIG. 3.
Combined stimulus-related and set-related responses, both of which were target dependent. Conventions as in Fig. 2. This PMd neuron showed phasic, stimulus-related discharge followed by tonic, set-related discharge on trials in which the right target had been desinated as the correct target by the IS. This directional selectivity was the same under both rotation conditions.
View larger version (53K):
[in a new window]
FIG. 4.
Limb-dependent set-related and movement-related responses. Conventions are the same as in Fig. 2. Under both rotation conditions, this PMd neuron showed tonic, set-related activity and phasic, early movement-related activity, both of which were maximal on trials that required leftward limb movments. Both responses were also characterized by reciprocal depression of discharge on trials that required rightward or backward limb movements, regardless of rotation condition. These responses were independent of target location.
and as "precue activity" by Vaadia et al. (1988) because it appears to anticipate predictable environmental events.
View larger version (47K):
[in a new window]
FIG. 5.
Combined anticipatory activity and target-dependent set-related activity. Conventions as in Fig. 2. This PMd neuron showed a pattern of tonic, nondirectional anticipatory discharge that began after center fixation point (CF) capture (not shown) and continued until shortly after the IS had been delivered (cue onset), followed by tonic, set-related activity that depended on the location of the designated target. The set-related discharge was maximal on trials in which the top target had been designated as the correct target, with reciprocal depression of discharge during the postinstruction period on trials in which either the right or bottom targets had been so designated. Both the directional, set-related activity and the nondirectional anticipatory activity were similar under both rotation conditions.
View larger version (48K):
[in a new window]
FIG. 6.
Anticipatory activity before IS onset in PMd. Layout is similar to Fig. 5, except that the neural data are aligned with CF (fixation) onset and with IS (cue) onset. Heavy dots: times of CF capture. This tonic, anticipatory discharge began with a gradual buildup of activity that began shortly after CF capture and continued until after the IS had been delivered. Apart from this anticipatory discharge, the cell showed no other task-related activity.
View larger version (41K):
[in a new window]
FIG. 7.
Target-dependent movement-related activity. Conventions as in Fig. 2, except that only the TS onset-aligned rasters and histograms are shown. Under both rotation conditions, this PMd neuron showed early movement-related activity that was maximal on trials in which either the bottom or left target had been designated for capture. The response was independent of limb trajectory. Also evident is the terminal portion of a weak set-related response that was target dependent, with maximal suppression of discharge on trials in which the bottom target had been designated for capture.
View larger version (49K):
[in a new window]
FIG. 8.
Limb-dependent movement-related activity. Conventions as in Fig. 7. This PMd neuron showed late movement-related activity that was maximal on trials that required rightward or backward movements, regardless of rotation condition. Neural response onset coincided with movement onset for backward hand trajectories, and was slightly earlier for rightward trajectories.
View larger version (57K):
[in a new window]
FIG. 9.
Target-dependent set-related activity combined with limb-dependent movement-related activity. Conventions as in Fig. 2, except that for both rotation conditions the 2nd set of rasters and histograms is aligned with movement onset rather than trigger onset. In the movement-aligned rasters, TS onsets are indicated by the heavy dots. This PMd neuron showed maximal set-related discharge on trials in which the left target was designated for capture, and reciprocal suppression of set-related activity on trials in which the right target was so designated. There was also a phasic, early movement-related discharge on trials that required either leftward or forward limb movements. The movement-related response was more difficult to discern because it was continuous with, and of the same magnitude as, the set-related discharge that preceded movements to capture the left target (bottom row). This cell also showed nondirectional anticipatory activity that began after CF capture (not shown) and ended with presentation of the visual IS (cue onset). All 3 types of activity were independent of rotation condition.
View larger version (37K):
[in a new window]
FIG. 10.
Complex set-related activity. This cell was tested initially in the rotated condition (A), then in the nonrotated condition (B), and finally in the rotated condition once again (C). For each rotation condition, rasters and histograms are aligned with IS (cue) onset. Heavy dots in the rasters: TS onsets, some of which occurred beyond the time window displayed here. This PMd neuron showed tonic, set-related discharge on trials in which leftward limb movements were required to capture the bottom target, but only during the rotated condition (3rd rows of A and C). In the nonrotated condition, there was no set-related response.
2 analysis of the relative frequencies of these three categories of directionally classifiable activity across the four task epochs showed that the apparent temporal changes were highly significant (2 = 63.96, df = 6, P = 7.02 × 10
12).
View larger version (55K):
[in a new window]
FIG. 11.
Bar plot showing numbers of PMd neurons with target-dependent, limb-dependent, or complex activity in each of the 4 task-defined epochs that followed IS onset. Stimulus-related activity occurred during the IS epoch, set-related activity during the delay epoch, early movement-related activity during the reaction time (RT) epoch, and late movement-related activity during the movement time (MT) epoch [see Table 1 of accompanying paper (Shen and Alexander 1997 )].
2 tests to partition the variance associated with the overall 2 analysis (Snedecor and Cochran 1989). Those results are presented in Table 2. Because of the apparent similarity in proportions of limb-dependent activity and complex activity across epochs (Table 1), we compared the frequencies of these two categories across epochs and found that they did not differ significantly (Table 2, row b: 2 = 2.15, df = 3, P = 0.46). Consequently, these two categories were combined, and their combined frequency was then compared with the frequency of target-dependent activity across epochs. The result (Table 2, row c: 2 = 62.58, df = 3, P = 1.65 × 1013) showed that nearly all of the variance in the overall 2 analysis could be accounted for by the difference across epochs in the frequencies of target-dependent versus limb-dependent plus complex activity.
View this table:
TABLE 2.
Task-related activity in PMd: frequency analysis of directionally classifiable activity across epochs
2 values for these last three comparisons (2 = 24.14, df = 3) was substantially less than the 2 for the comparable comparison across all epochs (Table 2, row c), because of the fact that the latter comparison also accounted for variance across nonadjacent epochs. This last point was illustrated by combining the corresponding frequencies of the first two epochs (IS and delay), and those of the last two epochs (RT and MT), and comparing the resulting frequencies across the two composite epochs. When the 2 resulting fromthis comparison (Table 2, row g: 2 = 49.65, df = 1, P =2.22 × 1016) was added to those obtained from the independent comparisons made across the first two epochs (IS vs. delay; Table 2, row d) and across the last two epochs (RT vs. MT; Table 2, row f), the sum of 2 values (2 = 65.32, df = 3) approximated that of the 2 for the comparable comparison across all epochs (Table 2, row c: 2 = 62.58, df = 3). The small residual difference is attributable to slight, but unavoidable, algebraic differences between the overall and partitioned analyses (Snedecor and Cochran 1989).
View larger version (11K):
[in a new window]
FIG. 12.
Surface diagrams of the PMd region explored in each monkey. Center of each circle marks the penetration site for each microelectrode track that contributed task-related responses to the final data base. Area of each circle is proportional to the number of neurons that contributed to the final data base along that track. The smallest circles represent 1 neuron per track. In monkey JA, the largest circle represents 12 neurons for that track. In monkey KO, the largest circles represent 6 neurons per track. The X- and Y-axes of each map (with scales in mm) correspond to the axes of the microdrive stage. AS, arcuate sulcus; CS, central sulcus; SPS, superior precentral sulcus.
). Figure 13 shows the comparative data in a normalized format.
View larger version (44K):
[in a new window]
FIG. 13.
Comparison across epochs of the relative frequencies of target- vs. limb-dependent responses in primary motor cortex (MC) vs. PMd. Bar plots for each region show normalized proportions of target-dependent, limb-dependent, and complex responses across the 4 task-defined epochs that followed IS onset. MC data were described separately in the accompanying paper (Shen and Alexander 1997 ). Conventions as in Fig. 11.
2 analysis. Because there were no significant differences in the relative frequencies of limb-dependent versus complex activity across any of the epochs, either for PMd (Tables 1 and 2) or for MC (Tables 3 and 4 of the accompanying paper (Shen and Alexander 1997), these two categories were combined and their combined frequency was compared with the frequency of target-dependent activity across the two cortical regions, epoch by epoch. The results are presented in Table 3. They indicate that there were significantly higher frequencies of target-dependent activity in PMd than in MC during the delay, RT, and MT epochs. During the IS epoch, the directionally classifiable (stimulus-related) activity was overwhelmingly target-dependent in both cortical regions (94% in each).
View this table:
TABLE 3.
Comparison of directionally classifiable activity in PMd and MC: frequency analysis within task epochs
DISCUSSION
Abstract
Introduction
Methods
Results
Discussion
References
) were collected from the same experimental animals invites direct comparisons of the task-related responses observed in these two regions. The parallels between the recruitment patterns observed in the two regions were striking. Both PMd and MC showed a predominance of target-dependent activity at the time of stimulus presentation, followed by increasing proportions of limb-dependent activity over the extended interval that concluded with the delayed motor response. In addition, both regions showed a corresponding increase in complex activity over this same interval. Within PMd, as within MC, the pattern of recruitment of limb-dependent activity was statistically indistinguishable from the pattern of recruitment of complex activity. These similarities in recruitment patterns suggest that both regions may participate in the spatial sensory-to-motor transformation required by the delayed reaching task.
; Dum and Strick 1991a; Kurata 1991; Muakkassa and Strick 1979; Tokuno and Tanji 1993) implies that much of the communication between these two cortical fields may be bidirectional. This is consistent with other recent evidence that tends to implicate PMd in earlier and more high-level processing
such as target representation and trajectory selectionthan MC, with the latter seeming to play a more direct role in specifying the moment-to-moment details of movement execution (Crammond and Kalaska 1996; Johnson et al. 1996).
) we suggested a simple framework for viewing the spatial sensorimotor transformation required by most tasks that involve visually instructed reaching: namely, as a chain or cascade of information processing leading from purely sensory processing to context-dependent or associative processing to purely motor processing. Neural correlates of purely sensory processing should reflect unconditionally some physical property of the sensory input, correlates of purely motor processing should reflect some physical property of the motor output, and correlates of associative processing should reflect some aspect of the behavioral context, being neither purely motor nor purely sensory.
, 1995; Kurata 1993; Riehle and Requin 1989), direction (or position) versus force (Bauswein et al. 1991; Riehle and Requin 1995; Riehle et al. 1994b; Werner et al. 1991), and direction versus endpoint (Caminiti et al. 1991). However, these studies were not designed to dissociate either spatial sensory variables (such as IS location) or spatial associative variables (such as instructed target location) from any of the purely motor variables that were being examined.
) or the location of the IS itself (Crammond and Kalaska 1994; diPellegrino and Wise 1993b). Hocherman and Wise (1991) sampled the task-related activity of PMd neurons in monkeys that had been trained to make reaching movements along three different trajectories to acquire the same spatial targets. They found that only a small proportion of the stimulus-, set-, and movement-related responses (7-9% of each) fulfilled their strict criteria for target selectivity by showing the same preferential response to a particular target location across all three trajectories of movement. However, in that study the spatial IS included not only a terminal target, which designated the endpoint for the reach, but also intermediate targets that specified the via points through which the trajectory was required to pass. By design, those intermediate targets or via points were not fully dissociated from the corresponding trajectories. It is possible, therefore, that the study may have underestimated the proportion of task-related responses that were actually target-dependent.
sampled neuronal activity from PMd in monkeys performing two delayed reaching tasks that dissociated the location of a visual IS from the spatial target of limb movement while target and limb trajectory were allowed to covary. The experimental design was complementary to that of the present study, in which the trajectory of limb movement was dissociated from the instructed target location while target and IS location were allowed to covary. Crammond and Kalaska found that only 8% of the directional set-related activity was IS-dependent, whereas 62% was either target- or limb-dependent. We found that only 8% of the directional set-related activity was limb dependent, whereas 76% was either IS- or target-dependent. The common variable that was left undissociated in both studies was target location. Because of the complementary designs of the two studies, their combined results suggest that the majority (54-68%) of the directional set-related activity observed in PMd may have been exclusively target dependent. The indicated range was obtained by subtracting the percentage of strictly limb-dependent activity identified in our present study from the percentage of either target- or limb-dependent activity identified in the study by Crammond and Kalaska (62% 
8%) and by subtracting the percentage of strictly IS-dependent activity observed in the latter study from the percentage of either IS- or target-dependent activity observed in ours (76% 8%).
sampled the task-related activity of rostral PMd neurons in a monkey that was trained to respond differentially to the same visuospatial stimuli (IS). In that study, the subject was required to maintain spatial attention directed toward one of eight radially arranged cue lights until the reillumination of the attended cue light triggered a reaching movement; the reach was directed either toward the previously instructed cue location (compatible condition) or in a fixed direction, regardless of cue location (incompatible condition). Thus across the two conditions the location of the IS was dissociated from the target or goal of the instructed limb movement. In the incompatible condition, DiPellegrino and Wise found that the majority of stimulus-related, set-related, and movement-related activity showed significant directional tuning in relation to IS location, and in some cases this tuning remained invariant across task conditions. Thus some of this activity may have been IS dependent or sensory in nature, according to the definitions employed in the present study.
, who used the population vector approach that was pioneered by Georgopoulos and colleagues (Caminiti et al. 1991; Georgopoulos 1995; Georgopoulos et al. 1984, 1988, 1989; Lurito et al. 1991). With the use of the preferred direction of each neuron computed from its RT activity during the compatible task, a population vector was calculated from the summed, activity-weighted contributions of all task-related neurons, assuming that each cell contributed to the population vector along the axis of its own preferred direction (Georgopoulos et al. 1986). In the incompatible task, the population vector pointed mainly toward the attended IS location throughout the postinstruction delay period, although it was deviated slightly toward the constant target of movement (i.e., toward the direction of the eventual motor response) by ~30% of the angular distance between IS and target. After the TS, the population vector shifted rapidly into alignment with the motor response. The authors concluded that the tonic deviation and eventual rotation of the population vector in the incompatible task was most likely to be accounted for by the graded recruitment of two separate categories of neuronal activity, one category being sensory/attentional and the other motor (i.e., limb-dependent) (Wise et al. 1997).
). Extensive sampling of task-related electromyographic activity throughout these experiments indicated that muscles of the proximal forelimb were essentially silent throughout the IS and delay epochs, and showed directional activations that covaried with limb trajectory during the early and late movement epochs. Although this argues against any simple relation between target-dependent neuronal responses and forelimb muscle activity, we cannot exclude the possibility that other muscles, which were not included among our sample, might have shown task-related activations that covaried with target location rather than limb trajectory.
has shown that ~80% of directional set-related responses in PMd may be modulated by the direction of gaze. Gaze effects could not explain the directional set-related activity recorded in the present study, however, because both monkeys maintained a relatively constant angle of gaze (fixating the center fixation point to detect its dimming) throughout the delay epoch. On the other hand, our eye position recordings did show that a saccade was made to the appropriate peripheral target immediately after the TS was presented. Because the direction of the saccade covaried with target location, it is possible that some of the target-dependent set- and/or movement-related activity may have been related to these target-directed eye movements, or to associated processes such as spatial attention. It is also possible that some of the target-dependent set-related activity may have been related to spatial memory for the location of the visual IS.
,b). This is consistent with the fact that rostral PMd receives direct input from dorsolateral prefrontal cortex (Lu et al. 1994), which has itself been strongly implicated in spatial memory processes (Funahashi et al. 1989, 1990, 1993; Fuster 1988; Joseph and Barone 1987; Niki and Watanabe 1976a) and is reciprocally connected with posterior parietal area 7a, known to play an important role in spatial attention (Mountcastle et al. 1981; Steinmetz and Constantinidis 1995; Steinmetz et al. 1994). On the other hand, there is little evidence that PMd has a direct or major role in oculomotor control, because neither lesions nor pharmacological manipulations nor microstimulation of this region have been reported to affect eye movements (Godschalk et al. 1995; Kurata and Hoffman 1994; Passingham 1985, 1986, 1989; Sawaguchi et al. 1996). Nevertheless, PMd does share reciprocal connections with the supplementary eye field (Huerta and Kaas 1990), which has been strongly implicated in the control of goal-directed saccades (Chen and Wise 1995a,b; Mushiake et al. 1996; Schall 1991; Schlag and Schlag-Rey 1987) and receives abundant inputs from various visuospatial processing areas (Huerta and Kaas 1990), including the dorsolateral prefrontal cortex and posterior parietal areas 7a, the lateral intraparietal area, and PO (Andersen et al. 1990; Colby et al. 1995; Galletti et al. 1991, 1993; Steinmetz et al. 1994). Recently it was shown that many supplementary eye field neurons are activated selectively when saccades are made with, rather than without, accompanying limb movements (Mushiake et al. 1996). PMd also receives direct inputs from posterior parietal areas, namely the medial intraparietal area and area 7m, both of which have been implicated in visuospatial processing (Cavada and Goldman-Rakic 1989; Chavis and Pandya 1976; Johnson et al. 1996; Kurata 1991; Petrides and Pandya 1984; Tokuno and Tanji 1993).
) were focused on PMd and MC, but it seems likely that other cortical motor fields may also contribute to spatial sensory-to-motor transformations of the type evoked in these experiments. Presently, at least eight distinct motor fields have been identified within primate frontal cortex (Dum and Strick 1991b; He et al. 1993, 1995; Luppino et al. 1991, 1993; Matsuzaka et al. 1992; Steinmetz and Constantinidis 1995), and these are differentiated by varying amounts and patterns of input from frontal and parietal visuospatial areas (Barbas and Pandya 1987; Cavada and Goldman-Rakic 1989; Chavis and Pandya 1976; Dum and Strick 1991a; Godschalk et al. 1984; Kurata 1991; Johnson et al. 1996; Matelli et al. 1986; Petrides and Pandya 1984; Tokuno and Tanji 1993; Vogt and Pandya 1987), varying contributions to direct, descending corticospinal pathways (He et al. 1993, 1995; Hummelsheim et al. 1986), and varying patterns of interconnections among themselves (Kurata 1991; Luppino et al. 1990, 1993; Morecraft and VanHoesen 1992; Tokuno and Tanji 1993). We hypothesize that within this distributed motor network, extrinsic, visually derived spatial information is gradually transformed into specific motor commands by a cascading sequence of sensory, associative, and motor processing that takes place both across and within the various cortical motor fields. Despite the reciprocity of many of the connections, the flow of spatial information through the network of cortical motor fields is hypothesized to depend largely on how direct or indirect are the connections that link each of the motor fields 1) with frontal and parietal visuospatial processing areas, 2) with other motor fields, and 3) with the segmental motor apparatus.
; Crammond and Kalaska 1994; diPellegrino and Wise 1993b; Hocherman and Wise 1991; Lurito et al. 1991; Niki and Watanabe 1976b; Riehle et al. 1994a). However, much more extensive and detailed assessments of the time-dependent distributions of sensory, associative, and motor representations across the various cortical motor fields will be needed to determine whether spatial sensory-to-motor transformations are indeed implemented in the manner proposed here.
| |
ACKNOWLEDGEMENTS |
|---|
This work was supported by National Institute of Neurological Disorders and Stroke Grant NS-17678.
| |
FOOTNOTES |
|---|
Address for reprint requests: G. E. Alexander, Dept. of Neurology, Emory University School of Medicine, 1639 Pierce Dr., P.O. Drawer V, Atlanta, GA 30322.
Received 28 February 1996; accepted in final form 7 November 1996.
| |
REFERENCES |
|---|
|
Abstract
Introduction
Methods
Results
Discussion
References
|
|---|
This article has been cited by other articles:
|
|
 |
|
  J. Rickert, A. Riehle, A. Aertsen, S. Rotter, and M. P. Nawrot Dynamic Encoding of Movement Direction in Motor Cortical Neurons J. Neurosci., November 4, 2009; 29(44): 13870 - 13882. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 G. Blohm, G. P. Keith, and J. D. Crawford Decoding the Cortical Transformations for Visually Guided Reaching in 3D Space Cereb Cortex, June 1, 2009; 19(6): 1372 - 1393. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
S. W. C. Chang, A. R. Dickinson, and L. H. Snyder Limb-Specific Representation for Reaching in the Posterior Parietal Cortex J. Neurosci., June 11, 2008; 28(24): 6128 - 6140. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J Duque, R Mazzocchio, K Stefan, F Hummel, E Olivier, and L. G. Cohen Memory Formation in the Motor Cortex Ipsilateral to a Training Hand Cereb Cortex, June 1, 2008; 18(6): 1395 - 1406. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 M. A. Lebedev, J. E. O'Doherty, and M. A. L. Nicolelis Decoding of Temporal Intervals From Cortical Ensemble Activity J Neurophysiol, January 1, 2008; 99(1): 166 - 186. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
B. M. Yu, C. Kemere, G. Santhanam, A. Afshar, S. I. Ryu, T. H. Meng, M. Sahani, and K. V. Shenoy Mixture of Trajectory Models for Neural Decoding of Goal-Directed Movements J Neurophysiol, May 1, 2007; 97(5): 3763 - 3780. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
E. Stark, I. Asher, and M. Abeles Encoding of Reach and Grasp by Single Neurons in Premotor Cortex Is Independent of Recording Site J Neurophysiol, May 1, 2007; 97(5): 3351 - 3364. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
A. J. Suminski, S. M. Rao, K. M. Mosier, and R. A. Scheidt Neural and Electromyographic Correlates of Wrist Posture Control J Neurophysiol, February 1, 2007; 97(2): 1527 - 1545. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
S. M. Beurze, F. P. de Lange, I. Toni, and W. P. Medendorp Integration of Target and Effector Information in the Human Brain During Reach Planning J Neurophysiol, January 1, 2007; 97(1): 188 - 199. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. M. Churchland, G. Santhanam, and K. V. Shenoy Preparatory Activity in Premotor and Motor Cortex Reflects the Speed of the Upcoming Reach J Neurophysiol, December 1, 2006; 96(6): 3130 - 3146. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
P. Cisek Preparing for Speed. Focus on "Preparatory Activity in Premotor and Motor Cortex Reflects the Speed of the Upcoming Reach" J Neurophysiol, December 1, 2006; 96(6): 2842 - 2843. [Full Text] [PDF]
|
|
|
|
|
|
Y. Aramaki, M. Honda, T. Okada, and N. Sadato Neural Correlates of the Spontaneous Phase Transition during Bimanual Coordination Cereb Cortex, September 1, 2006; 16(9): 1338 - 1348. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
E. Hoshi and J. Tanji Differential Involvement of Neurons in the Dorsal and Ventral Premotor Cortex During Processing of Visual Signals for Action Planning J Neurophysiol, June 1, 2006; 95(6): 3596 - 3616. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
R. Paz, C. Natan, T. Boraud, H. Bergman, and E. Vaadia Emerging Patterns of Neuronal Responses in Supplementary and Primary Motor Areas during Sensorimotor Adaptation J. Neurosci., November 23, 2005; 25(47): 10941 - 10951. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
L. E. Sergio, C. Hamel-Paquet, and J. F. Kalaska Motor Cortex Neural Correlates of Output Kinematics and Kinetics During Isometric-Force and Arm-Reaching Tasks J Neurophysiol, October 1, 2005; 94(4): 2353 - 2378. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
N. Saito, H. Mushiake, K. Sakamoto, Y. Itoyama, and J. Tanji Representation of Immediate and Final Behavioral Goals in the Monkey Prefrontal Cortex during an Instructed Delay Period Cereb Cortex, October 1, 2005; 15(10): 1535 - 1546. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
T. Ochiai, H. Mushiake, and J. Tanji Involvement of the Ventral Premotor Cortex in Controlling Image Motion of the Hand During Performance of a Target-capturing Task Cereb Cortex, July 1, 2005; 15(7): 929 - 937. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. A. Lebedev, J. M. Carmena, J. E. O'Doherty, M. Zacksenhouse, C. S. Henriquez, J. C. Principe, and M. A. L. Nicolelis Cortical Ensemble Adaptation to Represent Velocity of an Artificial Actuator Controlled by a Brain-Machine Interface J. Neurosci., May 11, 2005; 25(19): 4681 - 4693. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 S. Shipp The importance of being agranular: a comparative account of visual and motor cortex Phil Trans R Soc B, April 29, 2005; 360(1456): 797 - 814. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
E. Hoshi and J. Tanji Differential Roles of Neuronal Activity in the Supplementary and Presupplementary Motor Areas: From Information Retrieval to Motor Planning and Execution J Neurophysiol, December 1, 2004; 92(6): 3482 - 3499. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
U. Wolfensteller, R. I. Schubotz, and D. Y. von Cramon "What" Becoming "Where": Functional Magnetic Resonance Imaging Evidence for Pragmatic Relevance Driving Premotor Cortex J. Neurosci., November 17, 2004; 24(46): 10431 - 10439. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J. H. Fecteau, A. H. Bell, and D. P. Munoz Neural Correlates of the Automatic and Goal-Driven Biases in Orienting Spatial Attention J Neurophysiol, September 1, 2004; 92(3): 1728 - 1737. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
T. Harada, D. N. Saito, K.-I. Kashikura, T. Sato, Y. Yonekura, M. Honda, and N. Sadato Asymmetrical Neural Substrates of Tactile Discrimination in Humans: A Functional Magnetic Resonance Imaging Study J. Neurosci., August 25, 2004; 24(34): 7524 - 7530. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
E. Hoshi and J. Tanji Area-Selective Neuronal Activity in the Dorsolateral Prefrontal Cortex for Information Retrieval and Action Planning J Neurophysiol, June 1, 2004; 91(6): 2707 - 2722. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
Y. Ben-Shaul, R. Drori, I. Asher, E. Stark, Z. Nadasdy, and M. Abeles Neuronal Activity in Motor Cortical Areas Reflects the Sequential Context of Movement J Neurophysiol, April 1, 2004; 91(4): 1748 - 1762. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
X. Liu, E. Robertson, and R. C. Miall Neuronal Activity Related to the Visual Representation of Arm Movements in the Lateral Cerebellar Cortex J Neurophysiol, March 1, 2003; 89(3): 1223 - 1237. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
P. Cisek, D. J. Crammond, and J. F. Kalaska Neural Activity in Primary Motor and Dorsal Premotor Cortex In Reaching Tasks With the Contralateral Versus Ipsilateral Arm J Neurophysiol, February 1, 2003; 89(2): 922 - 942. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
L. E. Sergio and J. F. Kalaska Systematic Changes in Motor Cortex Cell Activity With Arm Posture During Directional Isometric Force Generation J Neurophysiol, January 1, 2003; 89(1): 212 - 228. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
T. Hanakawa, M. Honda, N. Sawamoto, T. Okada, Y. Yonekura, H. Fukuyama, and H. Shibasaki The Role of Rostral Brodmann Area 6 in Mental-operation Tasks: an Integrative Neuroimaging Approach Cereb Cortex, November 1, 2002; 12(11): 1157 - 1170. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
T. Ochiai, H. Mushiake, and J. Tanji Effects of Image Motion in the Dorsal Premotor Cortex During Planning of an Arm Movement J Neurophysiol, October 1, 2002; 88(4): 2167 - 2171. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
P. Cisek and J. F. Kalaska Modest Gaze-Related Discharge Modulation in Monkey Dorsal Premotor Cortex During a Reaching Task Performed With Free Fixation J Neurophysiol, August 1, 2002; 88(2): 1064 - 1072. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
L. Koski, A. Wohlschlager, H. Bekkering, R. P. Woods, M.-C. Dubeau, J. C. Mazziotta, and M. Iacoboni Modulation of Motor and Premotor Activity during Imitation of Target-directed Actions Cereb Cortex, August 1, 2002; 12(8): 847 - 855. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 M. A. Lebedev and S. P. Wise Insights into seeing and grasping: distinguishing the neural correlates of perception and action. Behav Cogn Neurosci Rev, June 1, 2002; 1(2): 108 - 129. [Abstract] [PDF]
|
|
|
|
|
|
E. Hoshi and J. Tanji Contrasting Neuronal Activity in the Dorsal and Ventral Premotor Areas During Preparation to Reach J Neurophysiol, February 1, 2002; 87(2): 1123 - 1128. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. N. Shadlen and W. T. Newsome Neural Basis of a Perceptual Decision in the Parietal Cortex (Area LIP) of the Rhesus Monkey J Neurophysiol, October 1, 2001; 86(4): 1916 - 1936. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
D. J. Crammond and J. F. Kalaska Prior Information in Motor and Premotor Cortex: Activity During the Delay Period and Effect on Pre-Movement Activity J Neurophysiol, August 1, 2000; 84(2): 986 - 1005. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J. Messier and J. F. Kalaska Covariation of Primate Dorsal Premotor Cell Activity With Direction and Amplitude During a Memorized-Delay Reaching Task J Neurophysiol, July 1, 2000; 84(1): 152 - 165. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. Rijntjes, C. Dettmers, C. Buchel, S. Kiebel, R. S. J. Frackowiak, and C. Weiller A Blueprint for Movement: Functional and Anatomical Representations in the Human Motor System J. Neurosci., September 15, 1999; 19(18): 8043 - 8048. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
K. Zhang and T. J. Sejnowski A Theory of Geometric Constraints on Neural Activity for Natural Three-Dimensional Movement J. Neurosci., April 15, 1999; 19(8): 3122 - 3145. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
K. Kurata and E. Hoshi Reacquisition Deficits in Prism Adaptation After Muscimol Microinjection Into the Ventral Premotor Cortex of Monkeys J Neurophysiol, April 1, 1999; 81(4): 1927 - 1938. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J. D. Coltz, M. T. V. Johnson, and T. J. Ebner Cerebellar Purkinje Cell Simple Spike Discharge Encodes Movement Velocity in Primates during Visuomotor Arm Tracking J. Neurosci., March 1, 1999; 19(5): 1782 - 1803. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M.T.V. Johnson, J. D. Coltz, M. C. Hagen, and T. J. Ebner Visuomotor Processing as Reflected in the Directional Discharge of Premotor and Primary Motor Cortex Neurons J Neurophysiol, February 1, 1999; 81(2): 875 - 894. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
I. Toni, N. D. Schluter, O. Josephs, K. Friston, and R. E. Passingham Signal-, Set- and Movement-related Activity in the Human Brain: An Event-related fMRI Study Cereb Cortex, January 1, 1999; 9(1): 35 - 49. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
R. S. Turner, S. T. Grafton, J. R. Votaw, M. R. Delong, and J. M. Hoffman Motor Subcircuits Mediating the Control of Movement Velocity: A PET Study J Neurophysiol, October 1, 1998; 80(4): 2162 - 2176. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
H. van Mier, L. W. Tempel, J. S. Perlmutter, M. E. Raichle, and S. E. Petersen Changes in Brain Activity During Motor Learning Measured With PET: Effects of Hand of Performance and Practice J Neurophysiol, October 1, 1998; 80(4): 2177 - 2199. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
S. H. Scott, L. E. Sergio, and J. F. Kalaska Reaching Movements With Similar Hand Paths but Different Arm Orientations. II. Activity of Individual Cells in Dorsal Premotor Cortex and Parietal Area 5 J Neurophysiol, November 1, 1997; 78(5): 2413 - 2426. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
L. Shen and G. E. Alexander Neural Correlates of a Spatial Sensory-To-Motor Transformation in Primary Motor Cortex J Neurophysiol, March 1, 1997; 77(3): 1171 - 1194. [Abstract] [Full Text] [PDF]
|
|
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
| Visit Other APS Journals Online |
