Eiichi Naito

Single-trial reconstruction of finger-pinch forces from human motor-cortical activation measured by near-infrared spectroscopy (NIRS)

Near-infrared spectroscopy (NIRS) has recently been used to measure human motor-cortical activation, enabling the classification of the content of a sensory-motor event such as whether the left or right hand was used. Here, we advance this NIRS application by demonstrating quantitative estimates of multiple sensory-motor events from single-trial NIRS signals. It is known that different degrees of sensory-motor activation are required to generate various hand/finger force levels. Thus, using a sparse linear regression method, we examined whether the temporal changes in different force levels could be reconstructed from NIRS signals. We measured the relative changes in oxyhemoglobin concentrations in the bilateral sensory-motor cortices while participants performed an isometric finger-pinch force production with their thumb and index finger by repeatedly exerting one of three target forces (25, 50, or 75% of the maximum voluntary contraction) for 12 s. To reconstruct the generated forces, we determined the regression parameters from the training datasets and applied these parameters to new test datasets to validate the parameters in the single-trial reconstruction. The temporal changes in the three different levels of generated forces, as well as the baseline resting state, could be reconstructed, even for the test datasets. The best reconstruction was achieved when using only the selected NIRS channels dominantly located in the contralateral sensory-motor cortex, and with a four second hemodynamic delay. These data demonstrate the potential for reconstructing different levels of external loads (forces) from those of the internal loads (activation) in the human brain using NIRS.

Efficient foot motor control by Neymar's brain.

How very long-term (over many years) motor skill training shapes internal motor representation remains poorly understood. We provide valuable evidence that the football brain of Neymar da Silva Santos Júnior (the Brasilian footballer) recruits very limited neural resources in the motor-cortical foot regions during foot movements. We scanned his brain activity with a 3-tesla functional magnetic resonance imaging (fMRI) while he rotated his right ankle at 1 Hz. We also scanned brain activity when three other age-controlled professional footballers, two top-athlete swimmers and one amateur footballer performed the identical task. A comparison was made between Neymar’s brain activity with that obtained from the others. We found activations in the left medial-wall foot motor regions during the foot movements consistently across all participants. However, the size and intensity of medial-wall activity was smaller in the four professional footballers than in the three other participants, despite no difference in amount of foot movement. Surprisingly, the reduced recruitment of medial-wall foot motor regions became apparent in Neymar. His medial-wall activity was smallest among all participants with absolutely no difference in amount of foot movement. Neymar may efficiently control given foot movements probably by largely conserving motor-cortical neural resources. We discuss this possibility in terms of over-years motor skill training effect, use-dependent plasticity, and efficient motor control.

Body representations in the human brain revealed by kinesthetic illusions and their essential contributions to motor control and corporeal awareness.

The human brain can generate a continuously changing postural model of our body. Somatic (proprioceptive) signals from skeletal muscles and joints contribute to the formation of the body representation. Recent neuroimaging studies of proprioceptive bodily illusions have elucidated the importance of three brain systems (motor network, specialized parietal systems, right inferior fronto-parietal network) in the formation of the human body representation. The motor network, especially the primary motor cortex, processes afferent input from skeletal muscles. Such information may contribute to the formation of kinematic/dynamic postural models of limbs, thereby enabling fast online feedback control. Distinct parietal regions appear to play specialized roles in the transformation/integration of information across different coordinate systems, which may subserve the adaptability and flexibility of the body representation. Finally, the right inferior fronto-parietal network, connected by the inferior branch of the superior longitudinal fasciculus, is consistently recruited when an individual experiences various types of bodily illusions and its possible roles relate to corporeal awareness, which is likely elicited through a series of neuronal processes of monitoring and accumulating bodily information and updating the body representation. Because this network is also recruited when identifying ones own features, the network activity could be a neuronal basis for self-consciousness.

Importance of human right inferior frontoparietal network connected by inferior branch of superior longitudinal fasciculus tract in corporeal awareness of kinesthetic illusory movement

It is generally believed that the human right cerebral hemisphere plays a dominant role in corporeal awareness, which is highly associated with conscious experience of the physical self. Prompted by our previous findings, we examined whether the right frontoparietal activations often observed when people experience kinesthetic illusory limb movement are supported by a large-scale brain network connected by a specific branch of the superior longitudinal fasciculus fiber tracts (SLF I, II, and III). We scanned brain activity with functional magnetic resonance imaging (MRI) while nineteen blindfolded healthy volunteers experienced illusory movement of the right stationary hand elicited by tendon vibration, which was replicated after the scanning. We also scanned brain activity when they executed and imagined right hand movement, and identified the active brain regions during illusion, execution, and imagery in relation to the SLF fiber tracts. We found that illusion predominantly activated the right inferior frontoparietal regions connected by SLF III, which were not substantially recruited during execution and imagery. Among these regions, activities in the right inferior parietal cortices and inferior frontal cortices showed right-side dominance and correlated well with the amount of illusion (kinesthetic illusory awareness) experienced by the participants. The results illustrated the predominant involvement of the right inferior frontoparietal network connected by SLF III when people recognize postural changes of their limb. We assume that the network bears a series of functions, specifically, monitoring the current status of the musculoskeletal system, and building-up and updating our postural model (body schema), which could be a basis for the conscious experience of the physical self.

Self-face recognition shares brain regions active during proprioceptive illusion in the right inferior fronto-parietal superior longitudinal fasciculus III network

Proprioception is somatic sensation that allows us to sense and recognize position, posture, and their changes in our body parts. It pertains directly to oneself and may contribute to bodily awareness. Likewise, ones face is a symbol of oneself, so that visual self-face recognition directly contributes to the awareness of self as distinct from others. Recently, we showed that right-hemispheric dominant activity in the inferior fronto-parietal cortices, which are connected by the inferior branch of the superior longitudinal fasciculus (SLF III), is associated with proprioceptive illusion (awareness), in concert with sensorimotor activity. Herein, we tested the hypothesis that visual self-face recognition shares brain regions active during proprioceptive illusion in the right inferior fronto-parietal SLF III network. We scanned brain activity using functional magnetic resonance imaging while twenty-two right-handed healthy adults performed two tasks. One was a proprioceptive illusion task, where blindfolded participants experienced a proprioceptive illusion of right hand movement. The other was a visual self-face recognition task, where the participants judged whether an observed face was their own. We examined whether the self-face recognition and the proprioceptive illusion commonly activated the inferior fronto-parietal cortices connected by the SLF III in a right-hemispheric dominant manner. Despite the difference in sensory modality and in the body parts involved in the two tasks, both tasks activated the right inferior fronto-parietal cortices, which are likely connected by the SLF III, in a right-side dominant manner. Here we discuss possible roles for right inferior fronto-parietal activity in bodily awareness and self-awareness.

Contribution of Neuroimaging Studies to Understanding Development of Human Cognitive Brain Functions

Humans experience significant physical and mental changes from birth to adulthood, and a variety of perceptual, cognitive and motor functions mature over the course of approximately 20 years following birth. To deeply understand such developmental processes, merely studying behavioral changes is not sufficient; simultaneous investigation of the development of the brain may lead us to a more comprehensive understanding. Recent advances in noninvasive neuroimaging technologies largely contribute to this understanding. Here, it is very important to consider the development of the brain from the perspectives of “structure” and “function” because both structure and function of the human brain mature slowly. In this review, we first discuss the process of structural brain development, i.e., how the structure of the brain, which is crucial when discussing functional brain development, changes with age. Second, we introduce some representative studies and the latest studies related to the functional development of the brain, particularly for visual, facial recognition, and social cognition functions, all of which are important for humans. Finally, we summarize how brain science can contribute to developmental study and discuss the challenges that neuroimaging should address in the future.

An empirical solution for over-pruning with a novel ensemble-learning method for fMRI decoding

BACKGROUNDnRecent functional magnetic resonance imaging (fMRI) decoding techniques allow us to predict the contents of sensory and motor events or participants mental states from multi-voxel patterns of fMRI signals. Sparse logistic regression (SLR) is a useful pattern classification algorithm that has the advantage of being able to automatically select voxels to avoid over-fitting. However, SLR suffers from over-pruning, in which many voxels that are potentially useful for prediction are discarded.nnnNEW METHODnWe propose an ensemble solution for over-pruning, called Iterative Recycling (iRec), in which sparse classifiers are trained iteratively by recycling over-pruned voxels.nnnRESULTSnOur simulation demonstrates that iRec can effectively rectify over-pruning in SLR and improve its classification accuracy. We also conduct an fMRI experiment in which eight healthy volunteers perform a finger-tapping task with their index or middle fingers. The results indicate that SLR with iRec (iSLR) can predict the finger used more accurately than SLR. Further, iSLR is able to identify a voxel cluster representing the finger movements in the biologically plausible contralateral primary sensory-motor cortices in each participant. We also successfully dissociated the regularly arranged representation for each finger in the cluster.nnnCONCLUSION AND COMPARISON WITH OTHER METHODSnTo the best of our knowledge, ours is the first study to propose a solution for over-pruning with ensemble-learning that is applicable to any sparse algorithm. In addition, from the viewpoint of machine learning, we provide the novel idea of using the sparse classification algorithm to generate accurate divergent base classifiers.

Feeling the force: Returning haptic signals influence effort inference during motor coordination

Our brain is known to automatically optimize effort expenditure during motor coordination, such that for example, during bimanual braking of a bicycle, a well-oiled brake will automatically be used more than a corroded, heavy brake. But how does our brain infer the effort expenditure? All previous motor coordination models have believed that the effort in a task is known precisely to our brain, solely from the motor commands it generates. Here we show that this belief is incorrect. Through experiments and simulation we exhibit that in addition to the motor commands, the returning haptic signals play a crucial role in the inference of the effort during a force sharing task. Our results thus elucidate a previously unknown sensory-motor association that has major ramifications for our understanding of motor coordination and provides new insights into how sensory modifications due to ergonomics, stroke and disease can affect motor coordination in humans.

Decoding sequential finger movements from preparatory activity in higher-order motor regions: a functional magnetic resonance imaging multi-voxel pattern analysis

Performing a complex sequential finger movement requires the temporally well‐ordered organization of individual finger movements. Previous behavioural studies have suggested that the brain prepares a whole sequence of movements as a single set, rather than the movements of individual fingers. However, direct neuroimaging support for this hypothesis is lacking and, assuming it to be true, it remains unclear which brain regions represent the information of a prepared sequence. Here, we measured brain activity with functional magnetic resonance imaging while 14 right‐handed healthy participants performed two types of well‐learned sequential finger movements with their right hands. Using multi‐voxel pattern analysis, we examined whether the types of the forthcoming sequence could be predicted from the preparatory activities of nine regions of interest, which included the motor, somatosensory and posterior parietal regions in each hemisphere, bilateral visual cortices, cerebellum and basal ganglia. We found that, during preparation, the activity of the contralateral motor regions could predict which of the two sequences would be executed. Further detailed analysis revealed that the contralateral dorsal premotor cortex and supplementary motor area were the key areas that contributed to the prediction consistently across participants. These contrasted with results from execution‐related brain activity where a performed sequence was successfully predicted from the activities in the broad cortical sensory‐motor network, including the bilateral motor, parietal and ipsilateral somatosensory cortices. Our study supports the hypothesis that temporary well‐organized sequences of movements are represented as a set in the brain, and that preparatory activity in higher‐order motor regions represents information about upcoming motor actions.

Improving Human Plateaued Motor Skill with Somatic Stimulation

Procedural motor learning includes a period when no substantial gain in performance improvement is obtained even with repeated, daily practice. Prompted by the potential benefit of high-frequency transcutaneous electrical stimulation, we examined if the stimulation to the hand reduces redundant motor activity that likely exists in an acquired hand motor skill, so as to further upgrade stable motor performance. Healthy participants were trained until their motor performance of continuously rotating two balls in the palm of their right hand became stable. In the series of experiments, they repeated a trial performing this cyclic rotation as many times as possible in 15 s. In trials where we applied the stimulation to the relaxed thumb before they initiated the task, most reported that their movements became smoother and they could perform the movements at a higher cycle compared to the control trials. This was not possible when the dorsal side of the wrist was stimulated. The performance improvement was associated with reduction of amplitude of finger displacement, which was consistently observed irrespective of the task demands. Importantly, this kinematic change occurred without being noticed by the participants, and their intentional changes of motor strategies (reducing amplitude of finger displacement) never improved the performance. Moreover, the performance never spontaneously improved during one-week training without stimulation, whereas the improvement in association with stimulation was consistently observed across days during training on another week combined with the stimulation. The improved effect obtained in stimulation trials on one day partially carried over to the next day, thereby promoting daily improvement of plateaued performance, which could not be unlocked by the first-week intensive training. This study demonstrated the possibility of effectively improving a plateaued motor skill, and pre-movement somatic stimulation driving this behavioral change.