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The role of Parietal Cortex in the Online Control of Hand Movement Trajectory: an Inactivation and a Case Report Study
Full text linkThe role of the Superior Parietal Lobule (SPL) of the primate brain in the control of hand and eye movements has been investigated through two experiments. In one experiment two macaque monkeys were trained to perform arm movements under two task conditions. In the first the animal performed direct reaches from a central location to one of 4 peripheral visual targets. In a second condition (50% of the trials) a sudden change of target location occurred, either during the hand reaction-time (RT) or at movement-time (MT) onset. The animals were required to adjust as fast as possible their hand trajectory to reach the second target location. A behavioral testing was performed before and after SPL inactivation. The inactivated area had previously been studied in the same task by recording the activity of 225 cells that showed modulation by hand position, speed and movement direction, as well as by saccadic signals. In separate sessions, unilateral and bilateral injections of the GABA-A agonist muscimol were performed within area 5 (PE/PEc) of the SPL. As control, physiological saline was injected in the same loci. Bilateral muscimol injections caused an increase of the hand RT and MT toward the first target in the direct reaches, and to both the first and second target in the corrected ones. In the latter, this resulted in an increase of the time necessary for the correction of the hand trajectory and in an elongation of the hand-path toward the first target location. During corrected reaches, an elongation of the eye RT to both first and second target was also observed, together with a change of eye-hand coupling, which could partially explain the hand reaching disorder. These results identify SPL as a crucial node in the on-line control of hand and eye movement, and highlight the role of an eye impairment in the emergence of the movement disorder characteristic of Optic Ataxia (OA). In a second experiment a patient with OA from unilateral tumor lesion of the right SPL and a group of 8 age-matched normal control subjects were asked to perform reaching movements from a central position to peripheral visual targets presented on a touch-screen. The subjects were also requested to perform a similar center-out task under isometric condition, where a force had to be applied to an isometric manipulandum in order to move a visual cursor from the center of the workspace to peripheral visual targets. Both tasks were 3 performed with and without central fixation (extrafoveal and foveal condition, respectively). The results show no major impairments in the temporal aspects of the movement (such as eye and hand RT and MT). On the contrary, in the extrafoveal condition the patient showed larger constant errors (CE) of the movement endpoints than controls in both the reaching and isometric task. In the foveal condition statistically higher CEs were observed only in the isometric task. The patient also showed a higher variability in the endpoints' position as compared to controls across all tested conditions. These results show that OA can emerge not only when a hand movement is performed, but also when only a force pulse of desired strength and direction has to be generated
Visually-guided correction of hand reaching movements: The neurophysiological bases in the cerebral cortex
No full textThe ability of human and non-human primates to make fast corrections to hand movement trajectories after a sudden shift in the target's location is a key feature of visuo-motor behavior. In healthy individuals, hand movements smoothly adapt to a change in target location without needing to complete the movement to the first target location, as typical of parietal patients. This finding indicates that the nervous system continuously monitors the visual scene and is able to integrate new information in order to produce an efficient motor response. In this paper, we review the kinematics, reaction times and muscle activity observed during the online correction of hand movements as well as the underlying neurophysiological processes studied through single-cell neural recordings in monkeys. Brain stimulation, lesion and imaging studies in humans are also discussed. We demonstrate that while online correction mechanisms strongly depend on the activity of a parieto-frontal network of which the posterior parietal cortex is a crucial node, these mechanisms proceed smoothly and are similar to what is observed during simple point-to-point movements. Online correction of hand movements would rely on feedforward and feedback mechanisms in the parietal cortex, as part of the activity within the fronto-parietal network for the planning and execution of visuo-motor tasks
Timing and communication of parietal cortex for visuomotor control
No full textIn both monkeys and humans, motor cognition emerges from a parietal-frontal network containing discrete dominant domains of visual, eye and hand signals, where neurons are responsible for goal and effector selection. Within these domains, the combination of different inputs shape the tuning properties of neurons, while local and long cortico-cortical connections outline the architecture of the distributed network and determine the conduction time underlying eye-hand coordination, necessary for visually guided operations in the action space. The analysis of the communication timing between parietal and frontal nodes of the network helps understanding the sensorimotor cortical delays associated to different functions, such as online control of movement and eye-hand coordination, and opens a new perspective to the study of the parieto-frontal interactions
Online control of hand trajectory and evolution of motor intention in the parietofrontal system
Full text linkThe frontal mechanisms of motor intention were studied in dorsal premotor and motor cortex of monkeys making direct reaches to visual targets and online corrections of hand trajectory, whenever a change of the target's location occurred. This study and our previous one of parietal cortex (Archambault et al., 2009) provide a picture on the evolution of motor intention and online control of movement in the parietofrontal system. In frontal cortex, significant relationships were found between neural activity and hand kinematics (position, speed, and movement direction). When a change of motor intention occurred, the activity typical of the movement to the first target smoothly evolved into that associated with the movement toward the second one, as observed during direct reaches. Under these conditions, parietal cells remained a more accurate predictor of hand trajectory than frontal ones. The time lags of neural activity with hand kinematics showed that motor, premotor, and parietal cortex were activated sequentially. After the first target's presentation and its change of location, the population activity signaled the change of motor plan before the hand moved to the initial target's position. This signaling occurred earlier in premotor than in motor and parietal cortex. Thus, premotor cortex encodes a higher-order command for the correction of motor intention, while parietal cortex seems responsible for estimating the kinematics of the motor periphery, an essential step to allow motor cortex to modify the hand trajectory. This indicates that the parietofrontal system can update an original and not-yet-accomplished motor plan during its execution
Posterior parietal cortex encoding of dynamic hand force underlying hand–object interaction
Full text linkMajor achievements of primate evolution are skilled hand-object interaction and tool use, both in part dependent on parietal cortex expansion. We recorded spiking activity from macaque inferior parietal cortex during directional manipulation of an isometric tool, which required the application of hand forces to control a cursor's motion on a screen. In areas PFG/PF, the activity of ∼70% neurons was modulated by the hand force necessary to implement the desired target motion, reflecting an inverse model, rather than by the intended motion of the visual cursor (forward model). The population vector matched the direction and amplitude of the instantaneous force increments over time. When exposed to a new force condition, that obliged the monkey to change the force output to successfully bring the cursor to the final target, the activity of a consistent subpopulation of neurons changed in an orderly fashion and, at the end of a "Wash-out" session, retained memory of the new learned association, at the service of predictive control of force. Our findings suggest that areas PFG/PF represent a crucial node of the distributed control of hand force, by encoding instantaneous force variations and serving as a memory reservoir of hand dynamics required for object manipulation and tool use. This is coherent with previous studies in humans showing the following: (1) impaired adaptation to a new force field under TMS parietal perturbation; (2) defective control of direction of hand force after parietal lesion; and (3) fMRI activation of parietal cortex during object manipulation requiring control of fine hand forces
Impairment of Online Control of Hand and Eye Movements in a Monkey Model of Optic Ataxia
No full textThe parietal mechanisms for online control of hand trajectory were studied by combining single-cell recording and reversible inactivation of superior parietal area 5 (PE/PEc; SPL) of monkeys while these made reaches and saccades to visual targets, when the target position changed unexpectedly. Neural activity was modulated by hand position, speed, and movement direction, and by pre- and/or postsaccadic signals. After bilateral muscimol injection, an increase in the hand reaction- and movement-time toward both the first and second targets was observed. This caused an increase in the time necessary for the trajectory correction, and therefore an elongation of the hand-path toward the first target location. Furthermore, hand trajectories were different in shape than control ones. An elongation of the eye reaction time to both first and second targets was also observed, which could partially explain the deficit of planning and correction of hand movement. These results identify the superior parietal lobule as a crucial node in the online control of hand and eye movement and highlight the role of the eye impairment in the emergence of the reaching disorder so far regarded as the hallmark of optic ataxia
Neural activity associated to joint-action during social cooperation in frontal and parietal cortex of macaque monkeys
No full textThe neural mechanisms related to the ability of humans and non-human primates to interact through joint-action are still poorly investigated. In the domain of motor functions, the study of goal-directed movement showed that no obligatory relationship exists between neural activity and movement, but rather movement-related activity is context-dependent and linked to different cognitive states. So far, neural activity in different cortical areas has been studied in a single brain in action, thus missing all information typical of interacting brains through a joint action task.
Two monkeys sat together in front of a display and they were trained in a center-out task in two intermingled conditions. In the first (SELF), each monkey had to move individually a visual cursor from a central position toward 8 different peripheral targets, by applying a force on an isometric joystick while its partner observed the action. In the second condition (cooperative joint action: COOP), both monkeys had to move their cursors together toward the same peripheral target, under the constraint of a maximum inter-cursor distance limit, which was visualized as an outlined circle incorporating the two cursors. Thus, in this context monkeys had to cooperate to reach a common goal.
Extracellular single-unit activity (SUA) was recorded from premotor cortex (PM) and inferior parietal lobule (IPL), simultaneously from homologous areas of both monkeys by using two multiple-electrode arrays.
Preliminary results showed that kinematic parameters, such as amplitude and direction of the force applied on the joystick, were overall similar in the COOP and SELF conditions. However, analysis of temporal aspects related to COOP trials showed a tendency of each monkey to adapt its own behavior in order to accommodate partner’s behaviour. In 540 PM and 258 IPL neurons studied during Reaction- and Movement Time, a 2-way ANOVA showed a significant difference of SUA between SELF and COOP conditions in 28.5 % PM and 22.1% IPL cells, and between final target directions in 42.6% PM and 39.2 % IPL cells with an interaction factor that resulted significant in 13.7% PM and 14.3% IPL cells. Therefore, in these areas similar actions performed in different social contexts (such as in absence or presence of social interactions), modulates SUA in a different way.
These findings represent a first step toward the description of the neural operations underlying motor functions in a cooperative context and suggest that within this action cooperation network different areas encode joint-action during different behavioural epochs
Local field potentials are influenced by cooperative joint-action in frontal and parietal cortex of macaque monkeys
No full textThe importance of social interaction in human and cultural evolution is οnly surpassed by the extreme complexity of social brain functions, making neural processes underlying social behavior difficult to study. Actions are identified as own or alien and in some cases alien actions trigger the same neural activity as own actions. However, evidence of neuronal activity associated to joint action in a social context is scant.
We studied extracellular local field potentials (LFPs:1-100 Hz) from premotor cortex (PM) and inferior parietal lobule (IPL) in two rhesus monkeys, during a joint-action task. Our goal was to determine not only the relationship between behavior and LFPs, but more importantly the context influence of an obligatory joint-action with a partner on neural activity.
Monkeys were trained in a center-out task in two conditions. In the first condition (SELF) each monkey, individually, had to move its cursor from the center toward a peripheral target, by applying a force on an isometric joystick, while the partner monkey observed the action. In the second condition (cooperative joint action: COOP), both monkeys had to move their cursors simultaneously toward the same peripheral target, constrained by a maximum inter-cursor distance limit visualized as an outlined circle encompassing the two cursors. Thus, in this condition they had to cooperate to reach a common goal.
We recorded neural activity from 236 PM and 166 IPL sites together with behavioral key events, simultaneously from homologous areas of both monkeys, by using two multiple-electrode arrays. Offline, we defined two epochs of interest, reaction time (RT: 0.2 s from target onset) and movement time (MT: 0.2 s from movement onset). For each trial we calculated the peak-to-peak LFP amplitude in each epoch. Finally we compared these values between the self-acting (SELF) and joint acting (COOP) and between peripheral target directions.
Behavioral analysis of reaction time and movement time showed that monkeys adapted their behavior during the joint-action condition in order to accommodate the partner’s behavior. A two way ANOVA showed a significant difference of LFP activity during RT or MT between SELF and COOP conditions in 25.8 % PM and 21.1% IPL sites and between peripheral target directions in 41.9% PM and 36.7 % IPL sites with an interaction factor that resulted significant in 11% PM and 13% IPL sites.
Our data show that there exists in the parieto-frontal system an action cooperation network which is set in motion during cooperative joint-action. We also show that LFP, reflecting cell assembly coordination, can disclose executive and higher-order neural processes
A visuomotor disorder in absence of movement: Optic ataxia generalizes to learnt isometric hand action
No full textIt is well known that parietal lobe lesions often result in Optic Ataxia (OA), a disorder in which patients make inaccurate reaches to visual targets. However, it is not clear if lesions of the cortical areas involved in sensorimotor transformation, such as PPC, result in similar reach defects regardless of the type of the sensory signals to be aligned, therefore of the specific remapping required.
We asked a patient with OA from a unilateral tumor lesion of the right superior parietal lobule (SPL) and a group of healthy age-matched control subjects to perform a conventional center-out task involving either natural reaching movements toward targets over a touchscreen, or a learnt isometric hand action as to move a visual cursor toward the same target by controlling the force applied on a isometric joystick. Both tasks were performed under two conditions, in the first subjects were allowed to move the eye to the visual targets, therefore hand movement was performed when targets were in central vision; in the second, subjects were requested to maintain fixation on a central target while reaching to eccentric ones.
Learnt isometric action was affected similarly to natural reaches in both central and peripheral vision, with abnormal endpoint errors and spatial dispersion of hand-guided cursor trajectories toward visual targets. Perceptual and motor components of hand errors were dissociated showing that OA consists of both spatial and motor components, since a field effect emerged in the process of target localization, in addition to a hand effect observed only when considering the motor components of OA.
This suggests that lesion of posterior parietal cortex affects sensory-motor transformations not only when they require a natural displacement of the hand, but also after learning a task in which visual signals about target location need to be aligned with information from force receptors, therefore regardless of the specific remapping required
Do non-human primates cooperate? Evidences of motor coordination during a joint action task in macaque monkeys
No full textHumans are intensively social primates, therefore many of their actions are dedicated to communication and interaction with other individuals. Despite the progress in understanding the cognitive and neural processes that allow humans to perform cooperative actions, in non-human primates only few studies have investigated the ability to interact with a partner in order to reach a common goal. These studies have shown that in naturalistic conditions animals engage in various types of social behavior that involve forms of mutual coordination and cooperation. However, little is known on the capacity of non-human primates to actively cooperate in a controlled experimental setting, which allows full characterization of the motor parameters underlying individual action and their change during motor cooperation. To this aim, we analyzed the behavior of three pairs of macaque monkeys trained to perform solo and joint-actions by exerting a force on an isometric joystick, as to move an individual or a common cursor toward visual targets on a screen. We found that during cooperation monkeys reciprocally adapt their behavior by changing the parameters that define the spatial and temporal aspects of their action, as to fine tune their joint effort, and maximize their common performance. Furthermore the results suggest that when acting together the movement parameters that specify each actor's behavior are not only modulated during execution, but also during planning. These findings provide the first quantitative description of action coordination in non-human primates during the performance of a joint action task
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