Motor imagery—Anatomical representation and electrophysiological characteristics

Experience and results of neuropsychological studies have shown that motor imagery can improve motor performance and enhance motor learning. In recent years several electro-physiological and functional imaging studies have investigated the physiological basis for this observation. In the present essay we review two of our recent studies, in which we compared motor imagery with motor preparation and motor execution. In the first we used positron emission tomography to describe their functional anatomy and in the second we employed electromyography, H-reflexes and transcranial magnetic stimulation to delineate their electrophysiological characteristics. Both studies demonstrated that motor imagery shares some characteristics with motor preparation and other, additional ones with motor execution. Thus it can be seen as a special form of motor behaviour, similar but distinct from both motor preparation and execution. This combination of mutual and distinct characteristics may be the key to its successful role in motor learning. Special issue dedicated to Dr. Herman Bachelard.     

Musical training induces functional plasticity in perceptual and motor networks: insights from resting-state FMRI

A number of previous studies have examined music-related plasticity in terms of multi-sensory and motor integration but little is known about the functional and effective connectivity patterns of spontaneous intrinsic activity in these systems during the resting state in musicians. Using functional connectivity and Granger causal analysis, functional and effective connectivity among the motor and multi-sensory (visual, auditory and somatosensory) cortices were evaluated using resting-state functional magnetic resonance imaging (fMRI) in musicians and non-musicians. The results revealed that functional connectivity was significantly increased in the motor and multi-sensory cortices of musicians. Moreover, the Granger causality results demonstrated a significant increase outflow-inflow degree in the auditory cortex with the strongest causal outflow pattern of effective connectivity being found in musicians. These resting state fMRI findings indicate enhanced functional integration among the lower-level perceptual and motor networks in musicians, and may reflect functional consolidation (plasticity) resulting from long-term musical training, involving both multi-sensory and motor functional integration.     

The utility of zebrafish for studies of the comparative biology of motor systems

Although zebrafish are best known as a model for studies of development, there is now a growing role for the model in studies of the functional organization of the nervous system, including studies of a variety of sensory systems, central processing, and motor output. The zebrafish has much to offer for such work because of the unique combination of genetics, optical methods, and physiology it allows. Here I illustrate, using three examples, the broad range of avenues along which zebrafish can inform us about motor systems. The examples include efforts to understand the functional organization and evolution of spinal interneurons, the role of mutants in informing us about motor dysfunction and human disease, and the ability to use the special features of zebrafish to explore strategies to restore function after injury. The most important aspects of these studies are evident only when they are placed in a comparative context, so they serve to highlight the power of zebrafish in studies of the comparative biology of motor control.     

Functional magnetic resonance imaging as a tool for investigating human cortical motor function.

Non-invasive functional magnetic resonance imaging (fMRI) mapping techniques sensitive to the local changes of blood flow, blood volume, and blood oxygenation which accompany neuronal activation have been widely used over the last few years to investigate the functional organization of human cortical motor systems, and specifically of the primary motor cortex. Validation studies have demonstrated a good correspondence between quantitative and topographic aspects of data acquired by fMRI and positron emission tomography. The spatial and temporal resolution affordable by fMRI has allowed to achieve new important information on the distributed representation of hand movements in multiple functional modules, and on the intensity and spatial extent of neural activation in the contralateral and ipsilateral primary motor cortex in relation to parametric and nonparametric aspects of movement and to the degree of handedness. Neural populations with different functional characteristics have been identified in anatomically defined regions, and the temporal aspects of the activation during voluntary movement tracked in different components of the motor system. Finally, this technique has proved useful to deepen our understanding of the neural basis of motor imagery, demonstrating increased activity in the primary motor cortex during mental representation of sequential finger movements.     

New concepts of the supplementary motor area

The supplementary motor area, although traditionally defined as a single motor area, is not viewed as including at least three different areas that can be distinguished anatomically and physiologically. The differential use of these three areas for various motor behaviors has been the subject of recent studies that are beginning to provide novel concepts of the functional differentiation of each area.     

Imaging the premotor areas

Recent imaging studies of motor function provide new insights into the organization of the premotor areas of the frontal lobe. The pre-supplementary motor area and the rostral portion of the dorsal premotor cortex, the 'pre-PMd', are, in many respects, more like prefrontal areas than motor areas. Recent data also suggest the existence of separate functional divisions in the rostral cingulate zone.     

Flagellar movement driven by proton translocation

The bacterial flagellar motor couples ion flow to rotary motion at high speed and with apparently fixed stoichiometry. The functional properties of the motor are quite well understood, but its molecular mechanism remains unknown. Recent studies of motor physiology, coupled with mutational and biochemical studies of the components, put significant constraints on the mechanism. Rotation is probably driven by conformational changes in membrane-protein complexes that form the stator. These conformational changes occur as protons move on and off a critical Asp residue in the stator protein MotB, and the resulting forces are applied to the rotor protein FliG.     

Changing perspectives on the functional organization of the segmental motor system

Results from a wide variety of recent studies on the architecture and innervation of skeletal muscles, the neuromechanical characteristics of motor units, and the properties and spinal reflex actions of muscle proprioceptors present a number of challenges to conventional views of the functional organization of the segmental motor system. To illustrate the nature of these challenges, studies directed toward several specific issues are reviewed. These include the functional subdivision of single muscles into two or more neuromuscular compartments; the patterns of synaptic input from peripheral afferent fibers to motoneurons innervating muscle units of different "type;" and the convergence in the segmental reflex pathways from muscle spindles and tendon organs to motoneurons.     

Motor cortex plasticity--from physiology to clinical neurology.

Neurophysiologic, neuroanatomic and neuroimaging studies conducted over the past two decades reveal that the cerebral cortex is functionally and structurally dynamic. The functional topography of the motor cortex can be modified by a variety of experimental manipulations, including peripheral or central injury, electrical stimulation, pharmocologic treatment or behavioral experience. Recent evidence demonstrates that functional alterations in motor cortex organization are accompanied by changes in dendritic and synaptic structure, as well as alterations in the regulation of cortical neurotransmitter systems. This article describes the state of the science regarding the main mechanisms implicated in the motor cortex plasticity, the main tools used for its investigation and the consequence of the recent discoveries on the therapeutic and rehabilitation procedures for the brain-injured persons.     

Motor systems

The field of motor control has broadened considerably over the past decade. Increasingly detailed information has accrued about the cellular and molecular processes involved in motor pattern generation and motor learning while, at the other extreme, the comparison of studies in humans and monkeys has begun to bridge the gap between cognitive and motor functions. The most striking feature of recent research has been the intense use of electrophysiological procedures in behaving monkeys and non-invasive imaging procedures in humans to elucidate details of sensory-motor transformations and the functional roles of different brain regions in the learning, planning and execution of movements.     

Motor Imagery Learning Modulates Functional Connectivity of Multiple Brain Systems in Resting State

Background

Learning motor skills involves subsequent modulation of resting-state functional connectivity in the sensory-motor system. This idea was mostly derived from the investigations on motor execution learning which mainly recruits the processing of sensory-motor information. Behavioral evidences demonstrated that motor skills in our daily lives could be learned through imagery procedures. However, it remains unclear whether the modulation of resting-state functional connectivity also exists in the sensory-motor system after motor imagery learning.

Methodology/Principal Findings

We performed a fMRI investigation on motor imagery learning from resting state. Based on previous studies, we identified eight sensory and cognitive resting-state networks (RSNs) corresponding to the brain systems and further explored the functional connectivity of these RSNs through the assessments, connectivity and network strengths before and after the two-week consecutive learning. Two intriguing results were revealed: (1) The sensory RSNs, specifically sensory-motor and lateral visual networks exhibited greater connectivity strengths in precuneus and fusiform gyrus after learning; (2) Decreased network strength induced by learning was proved in the default mode network, a cognitive RSN.

Conclusions/Significance

These results indicated that resting-state functional connectivity could be modulated by motor imagery learning in multiple brain systems, and such modulation displayed in the sensory-motor, visual and default brain systems may be associated with the establishment of motor schema and the regulation of introspective thought. These findings further revealed the neural substrates underlying motor skill learning and potentially provided new insights into the therapeutic benefits of motor imagery learning.     

Functions and structures of the motor cortices in humans

Humans and non-human primates have several motor areas. Exactly how many is a matter of current debate. A proper parcellation of motor areas must be based on correlated structural and functional differences. Recent studies indicate that the primary motor cortex may be, in reality, two areas (4a and 4p). Similarly, there are undoubtedly two or more cingulate motor areas and perhaps two supplementary motor areas. The homologies between human and monkey brains are striking in some cases, making monkey models of human motor cortices attractive. The doctrine of a strict ‘homuncular’ somatotopical organization of motor areas will have to be abandoned. The engagement of motor areas in different types of voluntary seems merely a matter of degree of activation rather than exclusive specific contributions.     

Gap junctional communication among motor and other neurons shapes patterns of neural activity and synaptic connectivity during development

We are studying the functional roles of neuronal gap junctional coupling during development, using motor neurons and their synapses with muscle fibers as a model system. At neuromuscular synapses, several studies have shown that the relative pattern of activity among motor inputs competing for innervation of the same target muscle fiber determines how patterns of innervation are sculpted during the first weeks after birth. We asked whether gap junctional coupling among motor neurons modulates the relative timing of motor neuron activity in awake, behaving neonatal mice. We found that the activity of motor neurons innervating the same muscle is temporally correlated perinatally, during the same period that gap junction-mediated electrical and dye coupling are present. In vivo blockade of gap junctions abolished temporal correlations in motor neuron activity, without changing overall motor behavior, motor neuron activity patterns or firing frequency. Together with preliminary studies in mice lacking gap junction protein Cx40, our data suggest that developmentally regulated gap junctional coupling among motor and other neurons affects the activity in nascent neural circuits and thus in turn affects synaptic connectivity. Dynamic monitoring of dye coupling can be used to explore this possibility in normal mice and in mice lacking gap junction proteins during embryonic and neonatal development.     

Motor learning in man: A review of functional and clinical studies

This chapter reviews results of clinical and functional imaging studies which investigated the time-course of cortical and subcortical activation during the acquisition of motor a skill. During the early phases of learning by trial and error, activation in prefrontal areas, especially in the dorsolateral prefrontal cortex, is has been reported. The role of these areas is presumably related to explicit working memory and the establishment of a novel association between visual cues and motor commands. Furthermore, motor associated areas of the right hemisphere and distributed cerebellar areas reveal strong activation during the early motor learning. Activation in superior-posterior parietal cortex presumably arises from visuospatial processes, while sensory feedback is coded in the anterior-inferior parietal cortex and the neocerebellar structures. With practice, motor associated areas of the left-hemisphere reveal increased activity. This shift to the left hemisphere has been observed regardless of the hand used during training, indicating a left-hemispheric dominance in the storage of visuomotor skills. Concerning frontal areas, learned actions of sequential character are represented in the caudal part of the supplementary motor area (SMA proper), whereas the lateral premotor cortex appears to be responsible for the coding of the association between visuo-spatial information and motor commands. Functional imaging studies which investigated the activation patterns of motor learning under implicit conditions identified for the first, a motor circuit which includes lateral premotor cortex and SMA proper of the left hemisphere and primary motor cortex, for the second, a cognitive loop which consists of basal ganglia structures of the right hemisphere. Finally, activity patterns of intermanual transfer are discussed. After right-handed training, activity in motor associated areas maintains during performance of the mirror version, but is increased during the performance of the original-oriented version with the left hand. In contrary, increased activity during the mirror reversed action, but not during the original-oriented performance of the untrained right hand is observed after left-handed training. These results indicate the transfer of acquired right-handed information which reflects the mirror symmetry of the body, whereas spatial information is mainly transferred after left-handed training. Taken together, a combined approach of clinical lesion studies and functional imaging is a promising tool for identifying the cerebral regions involved in the process of motor learning and provides insight into the mechanisms underlying the generalisation of actions.     

Coping with variability in small neuronal networks

Experimental and corresponding modeling studies indicate that there is a 2- to 5-fold variation of intrinsic and synaptic parameters across animals while functional output is maintained. Here, we review experiments, using the heartbeat central pattern generator (CPG) in medicinal leeches, which explore the consequences of animal-to-animal variation in synaptic strength for coordinated motor output. We focus on a set of segmental heart motor neurons that all receive inhibitory synaptic input from the same four premotor interneurons. These four premotor inputs fire in a phase progression and the motor neurons also fire in a phase progression because of differences in synaptic strength profiles of the four inputs among segments. Our work tested the hypothesis that functional output is maintained in the face of animal-to-animal variation in the absolute strength of connections because relative strengths of the four inputs onto particular motor neurons is maintained across animals. Our experiments showed that relative strength is not strictly maintained across animals even as functional output is maintained, and animal-to-animal variations in strength of particular inputs do not correlate strongly with output phase. Further experiments measured the precise temporal pattern of the premotor inputs, the segmental synaptic strength profiles of their connections onto motor neurons, and the temporal pattern (phase progression) of those motor neurons all in the same animal for a series of 12 animals. The analysis of input and output in this sample of 12 individuals suggests that the number (four) of inputs to each motor neuron and the variability of the temporal pattern of input from the CPG across individuals weaken the influence of the strength of individual inputs. Moreover, the temporal pattern of the output varies as much across individuals as that of the input. Essentially, each animal arrives at a unique solution for how the network produces functional output.     

Sensory Responses of Reinnervated Muscle Spindles

EXTENSIVE morphological, histochemical and electrophysiological studies have been made on skeletal muscles at varying stages of motor reinnervation. But in spite of the physiological significance of muscle receptors in controlling skeletal muscle activity, there have been no detailed studies of their reinnervation. We have therefore investigated the functional and structural characteristics of muscle spindles associated with their sensory reinnervation.     

Getting ready to move: transmitted information in the corticospinal pathway during preparation for movement

Corticospinal interactions are considered to play a key role in executing voluntary movements. Nonetheless several different studies have shown directly and indirectly that these interactions take place long before movement starts, when preparation for forthcoming movements dominates. When motor-related parameters are continuously processed in several premotor cortical sites, segmental circuitry is directly exposed to this processing via descending pathways which originate from these sites in parallel to descending fibers that derive from primary motor cortex. Recent studies have highlighted the functional role of these interactions in priming downstream elements for the ensuing motor actions. Time-resolved analysis has further emphasized the dynamic properties of pre-movement preparatory activity.     

Increased cerebral activity in Parkinson’s disease patients carrying the DRD2 TaqIA A1 allele during a demanding motor task: a compensatory mechanism?

Previous studies suggest that neuroimaging techniques are useful for detecting the effects of functional genetic polymorphisms on brain function in healthy subjects or in patients presenting with psychiatric or neurodegenerative conditions. Former evidence showed that individuals carrying risk alleles displayed broader patterns of brain activity during behavioural and cognitive tasks, despite being clinically comparable to non-carriers. This suggests the presence of compensatory brain mechanisms. In the present study, we investigated this effect in Parkinson's disease (PD) patients carrying the DRD2 TaqIA A1 allelic variant. This variant may confer an increased risk of developing the disease and/or influence the clinical presentation. During a complex sequential motor task, we evidenced by functional magnetic resonance imaging that A1 allele carriers activated a larger network of bilateral cerebral areas than non-carriers, including cerebellar and premotor regions. Both groups had similar clinical and demographic measures. In addition, their motor performance during the functional magnetic resonance experiment was comparable. Therefore, our conclusions, pending replication in a larger sample, seem to reflect the recruitment of compensatory cerebral resources during motor processing in PD patients carrying the A1 allele.     

Localizing Movement-Related Primary Sensorimotor Cortices with Multi-Band EEG Frequency Changes and Functional MRI

Electroencephalographic (EEG) oscillations in multiple frequency bands can be observed during functional activity of the cerebral cortex. An important question is whether activity of focal areas of cortex, such as during finger movements, is tracked by focal oscillatory EEG changes. Although a number of studies have compared EEG changes to functional MRI hemodynamic responses, we can find no previous research that relates the fMRI hemodynamic activity to localization of the multiple EEG frequency changes observed in motor tasks. In the present study, five participants performed similar thumb and finger movement tasks in parallel EEG and functional MRI studies. We examined changes in five frequency bands (from 5–120 Hz) and localized them using 256 dense-array EEG (dEEG) recordings and high-resolution individual head models. These localizations were compared with fMRI localizations in the same participants. Results showed that beta-band (14–30 Hz) desynchronizations (power decreases) were the most robust effects, appearing in all individuals, consistently localized to the hand region of the primary motor cortex, and consistently aligned with fMRI localizations.