Neuronal activity in the primate supplementary motor area and the primary motor cortex in relation to spatio-temporal bimanual coordination

Single neuronal activity was recorded from the supplementary motor area (SMA-proper and pre-SMA) and primary motor cortex (M1) in two Macaca fascicularis trained to perform a delayed conditional sequence of coordinated bimanual pull and grasp movements. The behavioural paradigm was designed to distinguish neuronal activity associated with bimanual coordination from that related to a comparable motor sequence but executed unimanually (left or right arm only). The bimanual and unimanual trials were instructed in a random order by a visual cue. Following the cue, there was a waiting period until presentation of a "go-signal", signalling the monkey to perform the instructed movement. A total of 143 task-related neurons were recorded from the SMA (SMA-proper, 62; pre-SMA, 81). Most SMA units (87%) were active in both unimanual contralateral and unimanual ipsilateral trials (bilateral neurons), whereas 9% of units were active only in unimanual contralateral trials and 3% were active only in unimanual ipsilateral trials. Forty-eight per cent of SMA task-related units were classified as bimanual, defined as neurons in which the activity observed in bimanual trials could not be predicted from that associated with unimanual trials when comparing the same events related to the same arm. For direct comparison, 527 neurons were recorded from M1 in the same monkeys performing the same tasks. The comparison showed that M1 contains significantly less bilateral neurons (75%) than the SMA, whereas the reverse was observed for contralateral neurons (22% in M1). The proportion of M1 bimanual cells (53%) was not statistically different from that observed in the SMA. The results suggest that both the SMA and M1 may contribute to the control of sequential bimanual coordinated movements. Interlimb coordination may then take place in a distributed network including at least the SMA and M1, but the contribution of other cortical and subcortical areas such as cingulate motor cortex and basal ganglia remains to be investigated.     

Dexterity in adult monkeys following early lesion of the motor cortical hand area: the role of cortex adjacent to the lesion

Infant monkeys were subjected to unilateral lesions of the motor cortex (mainly its hand representation). After maturation, they showed normal use of the contralateral hand for global grip movements. However, as compared with the ipsilateral hand, precision grip tasks requiring relatively independent finger movements were performed with less dexterity, particularly if adjustments of the wrist position were necessary. The purpose of this study was to investigate mechanisms which may be responsible for the rather well, although not complete, preservation of manipulative behaviour of these adult monkeys. To this end, the hand representations were mapped bilaterally with intracortical microstimulation in the mature monkeys, and the dexterity of both hands assessed quantitatively in a precision grip task. The behavioural effects of reversible inactivations of the primary (M1) and supplementary (SMA) motor cortical areas were then tested. The following were found. (i) The hand contralateral to the lesion exhibited subtle but significant dexterity deficits, as compared with the ipsilateral hand; the deficit was essentially for complex movements requiring dissociation of the thumb-index finger pinch from the other digits, involving also an arm rotation. (ii) Reversible inactivation of the M1 hand representation in the intact hemisphere dramatically impaired dexterity of the opposite hand without affecting the ipsilateral hand (contralateral to the early lesion). (iii) A relatively complete hand representation was found to occupy a new territory, medial to the old lesion. (iv) The role of this new displaced representation was crucial for the preserved dexterity of the opposite hand, as evidenced by its functional inactivation. In contrast, inactivation of both SMA cortices did not interfere with the manipulative behaviour. It is thus concluded that the preserved functional capacity of manipulations with the hand opposite the early lesion can be essentially attributed to a cortical reorganization around the old lesion. Under the present experimental conditions, contributions from either the SMA or the intact M1 appear not to be crucial.     

Effects of lesions in the mesial frontal cortex on bimanual co-ordination in monkeys

The hypothesis was tested that the mesial frontal cortex, including the supplementary motor area, is engaged in bimanual co-ordination. Three monkeys, trained in a well-co-ordinated bimanual pull-and-grasp task, were subjected to unilateral or bilateral lesions of the mesial frontal cortex. With unilateral lesions, the deficit consisted in a delay in movement initiation of the contralateral arm. With a bilateral lesion, the deficit was more pronounced with marked bilateral delays in movement onset and slowing in reaching. However, in the three monkeys bimanual co-ordination at the moment of goal achievement remained intact with an excellent temporal co-variation of the two limbs. In the two unilateral cases, an adaptive strategy developed after a few sessions, either by catching up during reaching with the limb contralateral to the lesion (monkey M1) or by delaying movement initiation of the limb ipsilateral to the lesion (monkey M2). This outcome is discussed in terms of Lashley's principle of motor equivalence, i.e. invariant goal achievement with variable means. Bilateral lesions led to a transient and near-total impairment in movement self-initiation when all external cues were absent. It is concluded that in monkeys the mesial frontal cortex does not play a crucial role in bimanual co-ordination but rather in movement initiation, especially when sensory cues are absent.     

Primary motor cortex is involved in bimanual coordination

Many voluntary movements involve coordination between the limbs. However, there have been very few attempts to study the neuronal mechanisms that mediate this coordination. Here we have studied the activity of cortical neurons while monkeys performed tasks that required coordination between the two arms. We found that most neurons in the primary motor cortex (MI) show activity specific to bimanual movements (bimanual-related activity), which is strikingly different from the activity of the same neurons during unimanual movements. Moreover, units in the supplementary motor area (SMA; the area of cortex most often associated with bimanual coordination) showed no more bimanual-related activity than units in MI. Our results challenge the classic view that MI controls the contralateral (opposite) side of the body and that SMA is responsible for the coordination of the arms. Rather, our data suggest that both cortical areas share the control of bilateral coordination.     

The effects of sleep loss on component movements of human motion.

Does sleep loss produce differential effects on component movements of motion? Without a control group, 19 college students were given "several special tests of perceptual and motor functions in a 5-day training period, in a 3-day sleep loss period, and in a 2-day recovery period." Manipulation and travel movements in a panel-control task, speed of performance in a test of bimanual and unimanual coordination, speed of discrete leg movements, and critical flicker frequency all decreased. Contacts in a test of hand steadiness showed irregular change. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Changing directions of forthcoming arm movements: neuronal activity in the presupplementary and supplementary motor area of monkey cerebral cortex

1. To understand roles played by two cortical motor areas, the presupplementary motor area (pre-SMA) and supplementary motor area (SMA), in changing planned movements voluntarily, cellular activity was examined in two monkeys (Macaca fuscata) trained to perform an arm-reaching task in which they were asked to press one of two target buttons (right or left) in three different task modes. 2. In the first mode (visual), monkeys were visually instructed to result and press either a right or left key in response to a forth coming trigger signal. In the second mode (stay), monkeys were required to wait for the trigger signal and press the same target key as pressed in preceding trials. In the third mode (shift), a 50 Hz auditory cue instructed the monkey to shift the target of the future reach from the previous target to the previous nontarget. 3. While the monkeys were performing this task, we recorded 399 task-related cellular activities from the SMA and the pre-SMA. Among them, we found a group of neurons that exhibited activity changes related specifically to shift trials (shift-related cells). The following properties characterized these 112 neurons. First, they exhibited activity changes after the onset of the 50-Hz auditory cue and before the movement execution when the monkeys were required to change the direction of forthcoming movement. Second, they were not active when the monkeys pressed the same key without changing the direction of the movements. Third, they were not active when the monkeys received the 50-Hz auditory cue but failed to change the direction of the movements by mistake. These observations indicate that the activity of shift-related cells is related to the redirection of the forthcoming movements, but not to the auditory instruction itself or to the location of the target key or the direction of the forthcoming movements. 4. Although infrequently, monkeys made errors in the stay trials and changed directions of the reach voluntarily. In that case, a considerably high proportion of shift-related neurons (12 of 19) exhibited significant activity changes long before initiation of the reach movement. These long-lasting activities were not observed during the preparatory period in correct stay trials, but resembled the shift-related activity observed when the target shift was made toward the same direction. Thus these activity changes were considered to be also related to the process of changing the intended movements voluntarily. 5. We found another population of neurons that showed activity modulation when the target shift was induced by the visual instruction in visual trials (visually guided shift-related neurons). These neurons were active when the light-emitting diode (LED) guided the forthcoming reach to the previous nontarget but not to the previous target. Therefore their activity was not a simple visual response to the LED per se. A majority of them also showed shift-related activity in shift trials (19 of 22 in monkey 2). 6. Neurons exhibiting the shift-related activity were distributed differentially among the two areas. In the pre-SMA, 31% of the neurons recorded showed the shift-related activity, whereas in the SMA, only 7% showed such an activity. These results suggest that pre-SMA and SMA play differential roles in updating the motor plans in accordance with current requirements.     

Bimanual interference associated with the selection of target locations.

Four experiments were conducted to identify the locus of interference observed during the preparation of bimanual reaching movements. Target locations were specified by color, and the right-hand and left-hand targets could be either the same or a different color. Movements of different amplitudes (Experiment 1) or different directions (Experiment 2) to targets of the same color were initiated more quickly than symmetric movements to targets of different colors. These results indicate that costs observed during bimanual movements arise during target selection rather than during motor programming. Experiments 3 and 4 further examined the interference associated with target selection. Reaction time costs were found with unimanual movements when the target was presented among distractors associated with responses for the other hand. Interference observed during bimanual reaching appears to reflect difficulty in segregating the response rules assigned to each hand. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Functional anatomy of pointing and grasping in humans

The functional anatomy of reaching and grasping simple objects was determined in nine healthy subjects with positron emission tomography imaging of regional cerebral blood flow (rCBF). In a prehension (grasping) task, subjects reached and grasped illuminated cylindrical objects with their right hand. In a pointing task, subjects reached and pointed over the same targets. In a control condition subjects looked at the targets. Both movement tasks increased activity in a distributed set of cortical and subcortical sites: contralateral motor, premotor, ventral supplementary motor area (SMA), cingulate, superior parietal, and dorsal occipital cortex. Cortical areas including cuneate and dorsal occipital cortex were more extensively activated than ventral occipital or temporal pathways. The left parietal operculum (putative SII) was recruited during grasping but not pointing. Blood flow changes were individually localized with respect to local cortical anatomy using sulcal landmarks. Consistent anatomic landmarks from MRI scans could be identified to locate sensorimotor, ventral SMA, and SII blood flow increases. The time required to complete individual movements and the amount of movement made during imaging correlated positively with the magnitude of rCBF increases during grasping in the contralateral inferior sensorimotor, cingulate, and ipsilateral inferior temporal cortex, and bilateral anterior cerebellum. This functional-anatomic study defines a cortical system for "pragmatic' manipulation of simple neutral objects.     

Hand preferences in unimanual and coordinated-bimanual tasks by tufted capuchin monkeys (Cebus apella).

Hand preferences in 26 capuchin monkeys (Cebus apella) were examined in 2 reaching-for-food tasks under 2 postural conditions. In the 1st task (unimanual), monkeys were required to reach for food from both a quadrupedal and an upright posture. A right-hand bias was found for the upright but not for the quadrupedal condition. In the 2nd task (coordinated bimanual), monkeys were required to extract the food from a hanging Plexiglas tube from both a crouched and an upright posture. A right-hand bias was found for both conditions. A significant increase in right-hand use was noted from the unimanual, quadrupedal, reaching task to the coordinated-bimanual task, with females exhibiting a greater right-hand preference than males. In addition, a significant effect of task complexity on strength in laterality was found. Results are discussed in the context of recent theories on primate laterality. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Hand preferences in unimanual and bimanual feeding by wild vervet monkeys (Cercopithecus aethiops).

Lateral preference was examined in spontaneous feeding actions in 2 troops of wild vervet monkeys (Cercopithecus aethiops). Processing of 4 foods (termites, leaf shoots, sugarcane, and fruit) was studied. Actions included unimanual reaching to moving objects, operating from an unstable posture, and coordinated bimanual processing. Between 19 and 31 subjects were available, according to the task. In 2 tasks, laterality of 2 independent stages was measured separately, giving 6 measures in all. On 4 of these measures, most monkeys were ambipreferent, and only a few showed significant hand preferences. Only for termite feeding and detaching material from fruits did the majority show significant lateralization; no tasks elicited exclusive use of 1 hand. Preference appeared labile, because in 2 tasks, population trends reversed with increasing age. No population trends to left or right were found; instead, these monkeys showed ambilaterality, with lateralization associated with task complexity. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Visual control of the arm, the wrist and the fingers: pathways through the brain

Sperry and his colleagues had shown that section of the corpus callosum blocks the normally strong interocular transfer of visual learning in chiasma sectioned monkeys. Although interhemispheric transfer of learning was blocked, monkeys could be readily trained to use any combination of eye and hand in a task that required rapid visually guided responses. Sperry suggested that there must be a subcortical pathway linking sensory to motor areas of the brain. We tested monkeys in a task which required them to orient their wrist and fingers correctly in order to remove a morsel of food from a slotted disc. Animals in which we made lesions of the dorsal extrastriate visual areas of the parietal lobe were profoundly impaired in performing this task, but showed no deficit in visual discrimination learning. A monkey with an extensive lesion of the ventral, temporal lobe extrastriate areas showed no deficit in the visuomotor task but was profoundly impaired in visual discrimination learning. Lesions of peri-arcuate cortex, a major cortical target of parietal lobe visual areas, produced only a mild deficit which was motor in character. We suggest that the visuomotor deficit caused by parietal lobe lesions is brought about by depriving the cerebellum of its cortical visual input.     

Both supplementary and presupplementary motor areas are crucial for the temporal organization of multiple movements

Both supplementary and presupplementary motor areas are crucial for the temporal organization of multiple movements. J. Neurophysiol. 80: 3247-3260, 1998. To study the involvement of the supplementary (SMA) and presupplementary (pre-SMA) motor areas in performing sequential multiple movements that are individually separated in time, we injected muscimol, a gamma-aminobutyric acid agonist, bilaterally into the part of each area that represents the forelimb. Two monkeys were trained to perform three different movements, separated by a waiting time, in four or six different orders. First, each series of movements was learned during five trials guided by visual signals that indicated the correct movements. The monkeys subsequently executed the three movements in the memorized order, without the visual signals. After the injection of muscimol (3 microliter, 5 micrograms/microliters in 10 min) into either the SMA or pre-SMA bilaterally, the animals started making errors in performing the sequence of movements correctly from memory. However, when guided with a visual signal, they could select and perform the three movements correctly. The impaired memory-based sequencing of movements worsened progressively with time until the animals could not perform the task. Yet they still could associate the visual signals with the different movements at that stage. In control experiments on two separate monkeys, we found that injections of the same amount of muscimol into either the SMA or pre-SMA did not cause problems with nonsequential reaching movement regardless of whether it was visually triggered or self-initiated. These results support the view that both the SMA and pre-SMA are crucially involved in sequencing multiple movements over time.     

Movement-related potential measures of different modes of movement selection in Parkinson's disease

Movement-related potentials were recorded preceding self-paced voluntary movements in patients with Parkinson's disease and in healthy subjects of the same age group. We compared the Readiness Potential preceding joystick movements in a fixed direction and preceding joystick movements in freely selected directions. In normal subjects the Readiness Potential amplitude was higher preceding freely selected movements than preceding movements in a fixed direction. The Readiness Potential in Parkinson patients failed to be modified by the different modes of movement selection. The modulation of the Readiness Potential by different ways of preparing for movement might be due to the supplementary motor area (SMA) being more strongly engaged by tasks requiring internal control of movements than by tasks that are externally structured. The results suggest that this task-dependent variation of SMA activity is reduced in Parkinson's disease. A failing capacity to adapt SMA activity to different task demands has previously been suggested by evidence from positron emission tomography studies using similar tasks.     

Functional imaging of human motor cortex at high magnetic field

1. We used conventional gradient echo magnetic resonance imaging (MRI) at high field strength (4 Tesla) to functionally image the right motor cortex in six normal human subjects during the performance of a sequence of self-paced thumb to digit oppositions with the left hand (contralateral task), the right hand (ipsilateral task), and both hands (bilateral task). 2. A localized increase in activity in the lateral motor cortex was observed in all subjects during the task. The area of activation was similar in the contralateral and bilateral tasks but 20 times smaller in the ipsilateral task. The intensity of activation was 2.3 times greater in the contralateral than the ipsilateral task.     

Specification of movement amplitudes for the left and right hands: Evidence for transient parametric coupling from overlapping-task performance.

Bimanual coordination tasks suggest transient cross-talk between concurrent specification processes for movements of the left and right hand that vanishes as the time for specification increases. In 2 experiments with overlapping and successive unimanual tasks, the hypothesis of transient coupling was examined for a psychological-refractory-period paradigm. Time for specification was manipulated by varying the delay between first and second signal (Experiment 1) and by precuing the first response (Experiment 2). Participants performed rapid reversal movements of same or different amplitudes with the left and right hands. With different amplitudes, reaction times (RTs) of the second responses were longer than with same amplitudes at short delays, and this disappeared at longer delays in Experiment 1. In Experiment 2, precuing also reduced the difference between RTs of second responses in same-amplitude and different-amplitude trials. These findings are consistent with the hypothesis of transient coupling during amplitude specification obtained with bimanual tasks. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Bimanual motor coordination in agenesis of the corpus callosum.

The nature and extent of deficiencies in bimanual motor coordination in individuals with agenesis of the corpus callosum (ACC) was studied using the computerized Bimanual Coordination Test (cBCT). Compared with previous bimanual tasks, the cBCT is more specifically reliant on interhemispheric interactions of lateralized motor control, allows more precise measurement, and permits examination of performance over a wider range of bimanual challenges. The cBCT performance of 13 high-functioning individuals with complete ACC was compared to 21 age- and IQ-matched controls. The groups did not differ in unimanual response speed. On trials involving angled paths that require bimanual coordination, the ACC group performed significantly slower and less accurately across all angles. The largest group differences in speed occurred on trials where the hands must respond symmetrically, while mirror-image (vs. parallel) responding produced the greatest deficits in accuracy. These data confirm previous findings of deficits in bimanual coordination in callosal absence, but using significantly improved measurement technology. Deficits in bimanual coordination in ACC are present across different demands for interhand interactions in the speed and direction of movement. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Asymétrie fonctionnelle haptique et efficience manuelle motrice chez l'enfant aveugle de 6 à 14 ans.

Studied the effects of age and handedness on the ability of blind children to discriminate Braille characters unimanually and to perform unimanual motor tasks. Human subjects: 48 male and female school-age children and adolescents (aged 6–14 yrs) (blindness). Each S was submitted to 2 series of unimanual tasks designed to measure the ability to (1) discriminate and recognize Braille characters unimanually (haptic efficiency) and (2) perform motor tasks involving tapping ability and grip-strength (motor efficiency). The time spent and number of errors in performing each task were evaluated according to the Ss' age, use of right or left hand, or use of both hands. An analysis of variance (ANOVA) and other statistical tests were used. (English abstract) (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Activity of common marmosets (Callithrix jacchus) in limited spaces: Hand movement characteristics.

The increasing popularity of marmoset monkeys (Callithrix jacchus) in anatomical, behavioral, and electrophysiological studies has called for a detailed analysis of their natural behavior within limited spaces. In the present study, the authors analyzed hand movements during horizontal and vertical progressions in a cylinder. The trajectory of each hand covered the entire cylinder floor during horizontal progressions and the entire cylinder wall during vertical progressions. Different marmosets have different patterns of hand movement. The average maximum angle of hand movements for all marmosets during horizontal and vertical progressions oscillates, although the average over time is constant and similar for both hands, whereas head movements during horizontal progressions become smaller with successive progressions. Another observed difference between rats and monkeys was in the size of head and hand movements at the beginning of each experimental session. During the 1st horizontal progression, all marmosets moved their heads to a greater extent than their hands. This sequential head and hand movement is referred as bistable behavior. The bistable pattern of motor behavior, which was also observed in successive progressions, may be derived from an inherent fear of predators or exploratory interest of a novel environment. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Manual preference for tapping in infants.

Used 2 tapping tasks to determine whether individual infants' right- or left-hand (RH and LH, respectively) preference for unimanual and bimanual tapping corresponded to their handedness in bimanual manipulation tasks (bimanual handedness) during the 2nd yr of life, and whether the developmental onset of a manual tapping preference occurred before or after the onset of bimanual handedness at the end of the 1st yr of life. At each of 2 age levels (15 and 22 mo, 24 Ss each), most infants demonstrated an RH preference in both tapping tasks, whether they showed bimanual right- or left-handedness. Nevertheless, a sizable minority of bimanual LH, but not RH, demonstrated an LH preference across tapping tasks. Since research with adults suggests left-hemisphere specialization for speech in almost all RH and many LH individuals, it is possible that a manual preference for tapping in infants, with appropriate empirical validation, will prove a reliable index of this specialization. In addition, 16 10-mo-olds demonstrated a manual preference in the unimanual tapping task whether they showed bimanual handedness, but few demonstrated a preference in the bimanual tapping task. This latter finding is consistent with past research using other handedness tasks with infants, which suggests that unimanual handedness precedes bimanual handedness. (19 ref) (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Production and characterization of profilin monoclonal antibodies

To evaluate the hypothesis that self-paced movements are mediated primarily by the supplementary motor area, whereas externally triggered movements are mainly affected by the lateral premotor cortex, different movements in 6 healthy volunteers were studied while changes in regional cerebral blood flow (rCBF) were measured using positron emission tomography (PET) and 15O-labeled water. Subjects made a series of finger opposition movements initiated in a self-paced manner every 4 to 6 seconds, and separately, made continuous finger opposition movements at a frequency of 2 Hz paced by a metronome. The primary motor cortex, lateral area 6, cerebellum on both sides, and caudal cingulate motor area, and the putamen and thalamus on the contralateral side were more active during the metronome-paced movements. The increases in rCBF in these areas are likely the result of the larger number of movements per minute made with the externally triggered task. The anterior supplementary motor area and rostral cingulate motor area in the midline, prefrontal cortices bilaterally, and lobus parietalis inferior on the ipsilateral side were more active during the self-paced movements. Increases in rCBF in those areas, which include medial premotor structures, may be related to the increased time devoted to planning the movement in this condition.