The hand is a marvellous organ. With our hands, we explore the world by contacting and manipulating the objects that we are interested in. The hand also presents one of the most complex structures in the body for its numerous degrees of freedom at the level of the joints and muscles. Because of these characteristics and for its peculiar shape, “the hand in action” is capable of complex skills. Due to the complexity of “the hand in action”, previous studies at first focused on classifying different hand postures and configurations based on anatomical and functional categorizations, considering the thumb, the fingers and the palm shaping in a huge range of motor tasks. Within a specific set of hand movements, multiple components were taken into account: the type of grip, the activation of muscle synergies, and in combination with object properties. An additional way to consider hand complexity was to count the number of muscles involved, the forces and the momentums produced, along with the neuromuscular connections. Indeed the act of prehension has been defined as "the application of functionally effective forces by the hand to an object for a task, given numerous biomechanical constraints". Aside from the behavioural and biomechanical studies, neuroscientists looked into the neurophysiology of the hand in action from a top-down perspective by focusing their attention on the brain-hand connection in order to investigate how such a complex apparatus is controlled. The main question then was: “How does the brain control the hands?” Actions have been shown to be represented in the brain during action execution, observation, and even during motor imagery. A neural model of the representation of movements was proposed to understand how action pre-planning can be transformed into a sequence of actual movements and where action representations are generated in the neural structures. Other lines of research have been followed to attempt to discover links between brain activity during mental imagery. Indeed, mental imagery, or motor imagery, is a pure mental state of an action, and can be considered as the ability to generate a conscious simulation of self-acting. Studying brain activity while a person is imagining performing an action, provides the opportunity to investigate how our motor system deals with planning in the absence of an actual action. These types of studies became available at the end of the past century when the development of new technology (e.g., fMRI and TMS) gradually overcame the difficulty of testing brain activity non-invasively. Since that time, studies significantly increased our understanding about the link between hand movements and relative brain activity. However, laboratory's studies limit the natural motor coordination as the one performed by people in everyday life. Grasping indeed is a complex action and its complexity is particularly expressed when the action is performed without constraints. This concept was well expressed by Newell and his model provides a valid perspective by suggesting that complex forms of motor behaviour could be viewed as products of self-organization arising from interactions between task, environment and organism constraints. Napier (1956) already recommended the necessity to incorporate as much complexity as possible in hand action when research is carried out. The core idea of the present study is to investigate the neural correlates of the hand in action during motor imagery. To address this issue, we will first deal with the studies that considered the hand’s shape in relation to its functions. Then we will tackle the problem from a neuronal level of analysis with particular attention to the studies that considered action imagination. Following this literature review, we will then point out some still-open questions and then state our research hypothesis. Two separate experiments will be described: “Grip-dependent cortico-spinal excitability during grasping imagination and execution” (Experiment 1), and “Motor system resonance for movement direction and amplitude during imagery and motor performance” (Experiment 2). Experiment 1 Studies converge in indicating a substantial similarity of the rules and mechanisms underlying execution, observation and imagery of actions, along with a large overlapping of their neural substrates. Recent transcranial magnetic stimulation (TMS) studies have demonstrated a muscle-specific facilitation of the observer’s motor system for force requirement and type of grip during grasping observation. However, whether similar fine-tuned muscle-specificity occurs even during imagination, when subjects are free to select the most convenient grip configuration, is still unknown. Here we applied TMS over the primary motor cortex and measured the corticospinal excitability (MEP) in three muscles (FDI, ADM and FDS) while subjects imagined grasping spheres of different dimensions and materials. This range of object weights and sizes allowed subjects to freely imagine the most suitable grip configuration among several possibilities. Activation measured during grasping imagination has been also compared to that obtained during real execution (EMG recorded from the same muscles). We found that during imagination of grasping small objects, the FDI muscle was more active than the ADM and the FDS, whereas the opposite pattern was found for big objects. Imagination of medium size objects, instead, required an equal involvement of the three muscles. The same pattern was observed when subjects were asked to perform the action. This suggests that during imagination, the cortico-spinal system is modulated in a muscle-specific/grip-specific way, as if the action would be really performed. However, when force was required (i.e. for the aluminum objects), the motor activation obtained during action execution was more fine-tuned to object dimensions than the activation recorded during imagination, suggesting a separate processing and control of force production. These findings underline a dissociation in grasp kinematics versus grasp kinetics depending on object properties. Experiment 2 Transcranial Magnetic Stimulation studies have shown that the motor system is facilitated by the sole imagination of motor actions. However, it is not clear whether the individual’s motor system resonates bilaterally and selectively for task parameters as movement direction and amplitude. To investigate this issue we apply a single pulse Transcranial Magnetic Stimulation (TMS) over the left and right primary motor cortex (M1) of healthy subjects that had to imagine to grasp and to rotate a clock hour hand, having a starting position at noon, toward four different hours: 2, 5, 7 and 10. Rotations toward 7 and 10 hours were in counter-clockwise direction, but required small movement amplitudes at 10 and large at 7 hour. Conversely, rotations toward 2 and 5 hours followed a clockwise direction and required small movement amplitude at 2 and a large at 5 hour. TMS motor evoked potentials were recorded from three hand muscles and movement imagined with the right and the left hand. Results showed that during motor imagery, the motor system activates the hand-intrinsic muscles specifically for movement direction by showing a mirroring pattern between the right and the left side of the motor cortex. Interestingly none muscle modulation, nor for hand-intrinsic or extrinsic, was observed for movement amplitude suggesting either that amplitude is modulated during the ongoing of the action or that selective inhibition is present in decreasing the otherwise elevated muscle activity evoked. We suggest that the plausibility of a movement is computed in regions upstream the primary motor cortex, and that motor imagery is a higher-order process not fully constrained by the rules that govern motor execution.
The hand is a marvellous organ. With our hands, we explore the world by contacting and manipulating the objects that we are interested in. The hand also presents one of the most complex structures in the body for its numerous degrees of freedom at the level of the joints and muscles. Because of these characteristics and for its peculiar shape, “the hand in action” is capable of complex skills. Due to the complexity of “the hand in action”, previous studies at first focused on classifying different hand postures and configurations based on anatomical and functional categorizations, considering the thumb, the fingers and the palm shaping in a huge range of motor tasks. Within a specific set of hand movements, multiple components were taken into account: the type of grip, the activation of muscle synergies, and in combination with object properties. An additional way to consider hand complexity was to count the number of muscles involved, the forces and the momentums produced, along with the neuromuscular connections. Indeed the act of prehension has been defined as "the application of functionally effective forces by the hand to an object for a task, given numerous biomechanical constraints". Aside from the behavioural and biomechanical studies, neuroscientists looked into the neurophysiology of the hand in action from a top-down perspective by focusing their attention on the brain-hand connection in order to investigate how such a complex apparatus is controlled. The main question then was: “How does the brain control the hands?” Actions have been shown to be represented in the brain during action execution, observation, and even during motor imagery. A neural model of the representation of movements was proposed to understand how action pre-planning can be transformed into a sequence of actual movements and where action representations are generated in the neural structures. Other lines of research have been followed to attempt to discover links between brain activity during mental imagery. Indeed, mental imagery, or motor imagery, is a pure mental state of an action, and can be considered as the ability to generate a conscious simulation of self-acting. Studying brain activity while a person is imagining performing an action, provides the opportunity to investigate how our motor system deals with planning in the absence of an actual action. These types of studies became available at the end of the past century when the development of new technology (e.g., fMRI and TMS) gradually overcame the difficulty of testing brain activity non-invasively. Since that time, studies significantly increased our understanding about the link between hand movements and relative brain activity. However, laboratory's studies limit the natural motor coordination as the one performed by people in everyday life. Grasping indeed is a complex action and its complexity is particularly expressed when the action is performed without constraints. This concept was well expressed by Newell and his model provides a valid perspective by suggesting that complex forms of motor behaviour could be viewed as products of self-organization arising from interactions between task, environment and organism constraints. Napier (1956) already recommended the necessity to incorporate as much complexity as possible in hand action when research is carried out. The core idea of the present study is to investigate the neural correlates of the hand in action during motor imagery. To address this issue, we will first deal with the studies that considered the hand’s shape in relation to its functions. Then we will tackle the problem from a neuronal level of analysis with particular attention to the studies that considered action imagination. Following this literature review, we will then point out some still-open questions and then state our research hypothesis. Two separate experiments will be described: “Grip-dependent cortico-spinal excitability during grasping imagination and execution” (Experiment 1), and “Motor system resonance for movement direction and amplitude during imagery and motor performance” (Experiment 2). Experiment 1 Studies converge in indicating a substantial similarity of the rules and mechanisms underlying execution, observation and imagery of actions, along with a large overlapping of their neural substrates. Recent transcranial magnetic stimulation (TMS) studies have demonstrated a muscle-specific facilitation of the observer’s motor system for force requirement and type of grip during grasping observation. However, whether similar fine-tuned muscle-specificity occurs even during imagination, when subjects are free to select the most convenient grip configuration, is still unknown. Here we applied TMS over the primary motor cortex and measured the corticospinal excitability (MEP) in three muscles (FDI, ADM and FDS) while subjects imagined grasping spheres of different dimensions and materials. This range of object weights and sizes allowed subjects to freely imagine the most suitable grip configuration among several possibilities. Activation measured during grasping imagination has been also compared to that obtained during real execution (EMG recorded from the same muscles). We found that during imagination of grasping small objects, the FDI muscle was more active than the ADM and the FDS, whereas the opposite pattern was found for big objects. Imagination of medium size objects, instead, required an equal involvement of the three muscles. The same pattern was observed when subjects were asked to perform the action. This suggests that during imagination, the cortico-spinal system is modulated in a muscle-specific/grip-specific way, as if the action would be really performed. However, when force was required (i.e. for the aluminum objects), the motor activation obtained during action execution was more fine-tuned to object dimensions than the activation recorded during imagination, suggesting a separate processing and control of force production. These findings underline a dissociation in grasp kinematics versus grasp kinetics depending on object properties. Experiment 2 Transcranial Magnetic Stimulation studies have shown that the motor system is facilitated by the sole imagination of motor actions. However, it is not clear whether the individual’s motor system resonates bilaterally and selectively for task parameters as movement direction and amplitude. To investigate this issue we apply a single pulse Transcranial Magnetic Stimulation (TMS) over the left and right primary motor cortex (M1) of healthy subjects that had to imagine to grasp and to rotate a clock hour hand, having a starting position at noon, toward four different hours: 2, 5, 7 and 10. Rotations toward 7 and 10 hours were in counter-clockwise direction, but required small movement amplitudes at 10 and large at 7 hour. Conversely, rotations toward 2 and 5 hours followed a clockwise direction and required small movement amplitude at 2 and a large at 5 hour. TMS motor evoked potentials were recorded from three hand muscles and movement imagined with the right and the left hand. Results showed that during motor imagery, the motor system activates the hand-intrinsic muscles specifically for movement direction by showing a mirroring pattern between the right and the left side of the motor cortex. Interestingly none muscle modulation, nor for hand-intrinsic or extrinsic, was observed for movement amplitude suggesting either that amplitude is modulated during the ongoing of the action or that selective inhibition is present in decreasing the otherwise elevated muscle activity evoked. We suggest that the plausibility of a movement is computed in regions upstream the primary motor cortex, and that motor imagery is a higher-order process not fully constrained by the rules that govern motor execution.
MOTOR SYSTEM RESONANCES IN COUPLING MUSCLES SYNERGIES AND TASK PARAMETERS
PIZZOLATO, Fabio
2011-01-01
Abstract
The hand is a marvellous organ. With our hands, we explore the world by contacting and manipulating the objects that we are interested in. The hand also presents one of the most complex structures in the body for its numerous degrees of freedom at the level of the joints and muscles. Because of these characteristics and for its peculiar shape, “the hand in action” is capable of complex skills. Due to the complexity of “the hand in action”, previous studies at first focused on classifying different hand postures and configurations based on anatomical and functional categorizations, considering the thumb, the fingers and the palm shaping in a huge range of motor tasks. Within a specific set of hand movements, multiple components were taken into account: the type of grip, the activation of muscle synergies, and in combination with object properties. An additional way to consider hand complexity was to count the number of muscles involved, the forces and the momentums produced, along with the neuromuscular connections. Indeed the act of prehension has been defined as "the application of functionally effective forces by the hand to an object for a task, given numerous biomechanical constraints". Aside from the behavioural and biomechanical studies, neuroscientists looked into the neurophysiology of the hand in action from a top-down perspective by focusing their attention on the brain-hand connection in order to investigate how such a complex apparatus is controlled. The main question then was: “How does the brain control the hands?” Actions have been shown to be represented in the brain during action execution, observation, and even during motor imagery. A neural model of the representation of movements was proposed to understand how action pre-planning can be transformed into a sequence of actual movements and where action representations are generated in the neural structures. Other lines of research have been followed to attempt to discover links between brain activity during mental imagery. Indeed, mental imagery, or motor imagery, is a pure mental state of an action, and can be considered as the ability to generate a conscious simulation of self-acting. Studying brain activity while a person is imagining performing an action, provides the opportunity to investigate how our motor system deals with planning in the absence of an actual action. These types of studies became available at the end of the past century when the development of new technology (e.g., fMRI and TMS) gradually overcame the difficulty of testing brain activity non-invasively. Since that time, studies significantly increased our understanding about the link between hand movements and relative brain activity. However, laboratory's studies limit the natural motor coordination as the one performed by people in everyday life. Grasping indeed is a complex action and its complexity is particularly expressed when the action is performed without constraints. This concept was well expressed by Newell and his model provides a valid perspective by suggesting that complex forms of motor behaviour could be viewed as products of self-organization arising from interactions between task, environment and organism constraints. Napier (1956) already recommended the necessity to incorporate as much complexity as possible in hand action when research is carried out. The core idea of the present study is to investigate the neural correlates of the hand in action during motor imagery. To address this issue, we will first deal with the studies that considered the hand’s shape in relation to its functions. Then we will tackle the problem from a neuronal level of analysis with particular attention to the studies that considered action imagination. Following this literature review, we will then point out some still-open questions and then state our research hypothesis. Two separate experiments will be described: “Grip-dependent cortico-spinal excitability during grasping imagination and execution” (Experiment 1), and “Motor system resonance for movement direction and amplitude during imagery and motor performance” (Experiment 2). Experiment 1 Studies converge in indicating a substantial similarity of the rules and mechanisms underlying execution, observation and imagery of actions, along with a large overlapping of their neural substrates. Recent transcranial magnetic stimulation (TMS) studies have demonstrated a muscle-specific facilitation of the observer’s motor system for force requirement and type of grip during grasping observation. However, whether similar fine-tuned muscle-specificity occurs even during imagination, when subjects are free to select the most convenient grip configuration, is still unknown. Here we applied TMS over the primary motor cortex and measured the corticospinal excitability (MEP) in three muscles (FDI, ADM and FDS) while subjects imagined grasping spheres of different dimensions and materials. This range of object weights and sizes allowed subjects to freely imagine the most suitable grip configuration among several possibilities. Activation measured during grasping imagination has been also compared to that obtained during real execution (EMG recorded from the same muscles). We found that during imagination of grasping small objects, the FDI muscle was more active than the ADM and the FDS, whereas the opposite pattern was found for big objects. Imagination of medium size objects, instead, required an equal involvement of the three muscles. The same pattern was observed when subjects were asked to perform the action. This suggests that during imagination, the cortico-spinal system is modulated in a muscle-specific/grip-specific way, as if the action would be really performed. However, when force was required (i.e. for the aluminum objects), the motor activation obtained during action execution was more fine-tuned to object dimensions than the activation recorded during imagination, suggesting a separate processing and control of force production. These findings underline a dissociation in grasp kinematics versus grasp kinetics depending on object properties. Experiment 2 Transcranial Magnetic Stimulation studies have shown that the motor system is facilitated by the sole imagination of motor actions. However, it is not clear whether the individual’s motor system resonates bilaterally and selectively for task parameters as movement direction and amplitude. To investigate this issue we apply a single pulse Transcranial Magnetic Stimulation (TMS) over the left and right primary motor cortex (M1) of healthy subjects that had to imagine to grasp and to rotate a clock hour hand, having a starting position at noon, toward four different hours: 2, 5, 7 and 10. Rotations toward 7 and 10 hours were in counter-clockwise direction, but required small movement amplitudes at 10 and large at 7 hour. Conversely, rotations toward 2 and 5 hours followed a clockwise direction and required small movement amplitude at 2 and a large at 5 hour. TMS motor evoked potentials were recorded from three hand muscles and movement imagined with the right and the left hand. Results showed that during motor imagery, the motor system activates the hand-intrinsic muscles specifically for movement direction by showing a mirroring pattern between the right and the left side of the motor cortex. Interestingly none muscle modulation, nor for hand-intrinsic or extrinsic, was observed for movement amplitude suggesting either that amplitude is modulated during the ongoing of the action or that selective inhibition is present in decreasing the otherwise elevated muscle activity evoked. We suggest that the plausibility of a movement is computed in regions upstream the primary motor cortex, and that motor imagery is a higher-order process not fully constrained by the rules that govern motor execution.
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