Distinct olfactory cross-modal effects on the human motor system

Background

Converging evidence indicates that action observation and action-related sounds activate cross-modally the human motor system. Since olfaction, the most ancestral sense, may have behavioural consequences on human activities, we causally investigated by transcranial magnetic stimulation (TMS) whether food odour could additionally facilitate the human motor system during the observation of grasping objects with alimentary valence, and the degree of specificity of these effects.

Methodology/Principal Findings

In a repeated-measure block design, carried out on 24 healthy individuals participating to three different experiments, we show that sniffing alimentary odorants immediately increases the motor potentials evoked in hand muscles by TMS of the motor cortex. This effect was odorant-specific and was absent when subjects were presented with odorants including a potentially noxious trigeminal component.The smell-induced corticospinal facilitation of hand muscles during observation of grasping was an additive effect which superimposed to that induced by the mere observation of grasping actions for food or non-food objects. The odour-induced motor facilitation took place only in case of congruence between the sniffed odour and the observed grasped food, and specifically involved the muscle acting as prime mover for hand/fingers shaping in the observed action.

Conclusions/Significance

Complex olfactory cross-modal effects on the human corticospinal system are physiologically demonstrable. They are odorant-specific and, depending on the experimental context, muscle- and action-specific as well. This finding implies potential new diagnostic and rehabilitative applications.     

Self and other in the human motor system

Observation of another's action can selectively facilitate the brain's motor circuits for making the same action . A "mirror-matching mechanism" might map observed actions onto the observer's own motor representations . Crucially, this view suggests that the brain represents others' actions like one's own. However, this hypothesis has been difficult to test because the experience of one's own body differs from that of others' bodies with respect to viewpoint, morphological features, familiarity, and the hallmark feature of kinaesthetic experience. We used an established method for manipulating the sense of body ownership ("rubber-hand illusion") to compare effects of observing actions that either were or were not illusorily attributed to the subject's own body. We show that observing another's actions facilitated the motor system, whereas observing identical actions, which were illusorily attributed to the subject's own body, showed the opposite pattern. Thus, motor facilitation strongly depends on the agent to whom the observed action is attributed. This result contradicts previous concepts of equivalence between one's own actions and actions of others and suggests that social differentiation, not equivalence, is characteristic of the human action system.     

Age-related changes in the activity of the human motor system

By analysis of parameters of isometric force recorded in healthy subjects from different age groups, amplitude and frequency changes in the integrated activity of motor system structures were shown to depend on voluntarily maintained isometric effort and its duration.     

Startle stimuli exert opposite effects on human cortical and spinal motor system excitability in leg muscles

Increased excitability of the spinal motor system has been observed after loud and unexpected acoustic stimuli (AS) preceding H-reflexes. The paradigm has been proposed as an electrophysiological marker of reticulospinal tract activity in humans. The brainstem reticular formation also maintains dense anatomical interconnections with the cortical motor system. When a startling AS is delivered, prior to transcranial magnetic stimulation (TMS), the AS produces a suppression of motor evoked potential (MEP) amplitude in hand and arm muscles of healthy subjects. Here we analyzed the conditioning effect of a startling AS on MEP amplitude evoked by TMS to the primary motor leg area. Ten healthy volunteers participated in two experiments that used a conditioning-test paradigm. In the first experiment, a startling AS preceded a suprathreshold transcranial test stimulus. The interstimulus interval (ISI) varied between 20 to 160 ms. When given alone, the test stimulus evoked a MEP amplitude of approximately 0.5 mV in the slightly preinervated soleus muscle (SOL). In the second experiment, the startling AS was used to condition the size of the H-reflex in SOL muscle. Mean MEP amplitude was calculated for each ISI. The conditioning AS suppressed MEP amplitude at ISIs of 30-80 ms. By contrast, H-reflex amplitude was augmented at ISIs of 100-200 ms. In conclusions, acoustic stimulation exerts opposite and ISI-specific effects on the amplitude of MEPs and H-reflex in the SOL muscle, indicating different mechanism of auditory-to-motor interactions at cortical and spinal level of motor system.     

Variations in the output impedance of the human motor system

The hypothesis that the properties of the stretch reflex could be changed dependent on the appointed task of the motor system was tested by measuring the mechanical output impedance of the hand of a human subject. Small disturbing torques were exerted on the hand rotating in the wrist joint in palmar and dorsal direction. The angular position, velocity and acceleration were recorded during 180 msec after the start of the disturbing torque. Within the linear range differences were found between the situations that (1) the subject kept his hand in a fixed position (posture) and (2) the subject tracked a simple and slow moving target (tracking). A simple model of the peripheral part of the motor system with the spinal reflex mechanism was made to analyse the responses. With the help of this model the changes in the reflex sensors were distinguished from changes in the mechanical system of the hand with the muscles attached to it and from changes in the effect of an activation of the muscle. During posture the responses were affected by the attention of the subject. An important part of these changes was a shift in the delay time of the reflex. During tracking the responses changed markely dependent on the velocity of the hand. When this velocity is larger than about 0.05 rad.sec^?1 then the strength of the reflex is approximately suppressed to about a half of the value during posture. Above this velocity the mechanical system of the hand with the muscles attached to it appeared to be less damped. The suppression of the reflex is caused by a decrease of the gain of the feedback sensors to about a third and an increase in the gain of the system of muscles with their load to about one and a half. It was concluded that the gain of the feedback sensors is controlled by signals from supraspinal levels.     

Physiological and pathological oscillatory networks in the human motor system.

Human brain functions are heavily contingent on neural interactions both at the single neuron and the neural population or system level. Accumulating evidence from neurophysiological studies strongly suggests that coupling of oscillatory neural activity provides an important mechanism to establish neural interactions. With the availability of whole-head magnetoencephalography (MEG) macroscopic oscillatory activity can be measured non-invasively from the human brain with high temporal and spatial resolution. To localise, quantify and map oscillatory activity and interactions onto individual brain anatomy we have developed the 'dynamic imaging of coherent sources' (DICS) method which allows to identify and analyse cerebral oscillatory networks from MEG recordings. Using this approach we have characterized physiological and pathological oscillatory networks in the human sensorimotor system. Coherent 8 Hz oscillations emerge from a cerebello-thalamo-premotor-motor cortical network and exert an 8 Hz oscillatory drive on the spinal motor neurons which can be observed as a physiological tremulousness of the movement termed movement discontinuities. This network represents the neurophysiological substrate of a discrete mode of motor control. In parkinsonian resting tremor we have identified an extensive cerebral network consisting of primary motor and lateral premotor cortex, supplementary motor cortex, thalamus/basal ganglia, posterior parietal cortex and secondary somatosensory cortex, which are entrained in the tremor or twice the tremor rhythm. This low frequency entrapment of motor areas likely plays an important role in the pathophysiology of parkinsonian motor symptoms. Finally, studies on patients with postural tremor in hepatic encephalopathy revealed that this type of tremor results from a pathologically slow thalamocortical and cortico-muscular coupling during isometric hold tasks. In conclusion, the analysis of oscillatory cerebral networks provides new insights into physiological mechanisms of motor control and pathophysiological mechanisms of tremor disorders.     

Immediate and long-term effects of radiation on the immune system of specific-pathogen-free mice

Studies on the immediate and long-term effects of radiation on the immune system of specific-pathogen-free mice are summarized in this paper. There was a striking difference in the radiation response of lymphocyte subsets; B cells consist of a fairly radiosensitive homogeneous population, whereas T cells consist of a large percentage (greater than 90 per cent) of radiosensitive and a small percentage (less than 10 per cent) of extremely radioresistant subpopulations. Ly 1+ and Ly 2+ lymphocytes appear equally radiosensitive, although the percentage of radioresistant cells was slightly larger for the former (approximately 5.5 per cent) than the latter (approximately 2.5 per cent). There was a significant strain difference in the radiosensitivity of immune-response potential in mice; immunocompetent cells of C3H mice were more radioresistant than those of BALB/c, C57BL/6, and B10.BR mice. Studies on the long-term effect of radiation on immune system in mice indicated no evidence for accelerated ageing of the immunologic functions when radiation exposure was given to young adults. Preliminary results on the enhancing effect of low dose radiation on cytotoxic T cell response in vitro are also discussed.     

Immediate effects of co-contraction training on motor control of the trunk muscles in people with recurrent low back pain

Although deficits in the activation of abdominal muscles are present in people with low back pain (LBP), this can be modified with motor training. Training of deep abdominal muscles in isolation from the other trunk muscles, as an initial phase of training, has been shown to improve the timing of activation of the trained muscles, and reduce symptoms and recurrence of LBP. The aim of this study was to determine if training of the trunk muscles in a non-isolated manner can restore motor control of these muscles in people with LBP. Ten subjects with non-specific LBP performed a single session of training that involved three tasks: “abdominal curl up”, “side bridge” and “birdog”. Electromyographic activity (EMG) of trunk and deltoid muscles was recorded with fine-wire and surface electrodes during rapid arm movements and walking, before and immediately following the intervention. Onset of trunk muscle EMG relative to that of the prime mover (deltoid) during arm movements and the mean, standard deviation (SD) and coefficient of variation of abdominal muscle EMG during walking were calculated. There was no significant change in the times of onset of trunk muscle EMG during arm movements nor was there any change in the variability of EMG of the abdominal muscles during walking. However, the mean amplitude and SD of abdominal EMG was reduced during walking after training. The results of this study suggest that unlike isolated voluntary training, co-contraction training of the trunk muscles does not restore the motor control of the deep abdominal muscles in people with LBP after a single session of training.     

Immediate effects of tobramycin on human cochlea and correlation with serum tobramycin levels.

Electrocochleography was performed on three patients to monitor the intravenous administration of tobramycin. When peak serum tobramycin levels exceeded 8-10 mug/ml an immediate dramatic reduction in cochlear output was observed, which recovered fully as serum levels fell. The patients had no auditory or vestibular symptoms either during or after treatment.     

Topical problems in the study of remote effects of chemical compounds on the cardiovascular system

The main tasks in epidemiological and experimental study of remote effects on the cardiovascular system of exposure to chemical compounds were formulated. In the epidemiological respect, the most important points are development of methods for integral evaluation of the effect of the environment, including the industrial environment, and improvement of the methods of detecting early signs of cardiovascular pathology closely correlating with the structure of cardiovascular morbidity and mortality. The most topical experimental problem is to refine the criteria and methods of assessing the state of the heart and vessels of experimental animals so as to make possible a substantiated and adequate extrapolation of experimental data to man.     

Event-related neuronal responses in the human strio-pallido-thalamic system. I. Sensory and motor functions

Multiunit activity was recorded from strio-pallido-thalamic sites in parkinsonian patients bearing gold electrodes for diagnosis and therapy. The patients voluntarily participated in tasks designed to study neuronal correlates of both physical and semantic characteristics of stimuli as well as motor responses. Six modifications of the stimulus-response paradigm were used: visual odd-ball, visual and acoustic odd-ball tasks; tasks in which either the stimulus intensity or the meaning of non-target stimuli varied; single-stage delayed response and dual-stage delayed response tasks, respectively. In each task the patients had to evaluate some of the stimulus characteristics and to respond in a particular way according to the preliminary instructions. Peristimulus time histograms for each multiunit separately as well as profiles of reactions and profiles of reaction differences for the whole set of multiunits were calculated and subjected to statistical analysis. Two functional groups of subcortical neuronal reactions, stimulus-related and response-related activities, were separated. The stimulus-related activities of most multiunits were modality-unspecific. Their most striking feature was dependence on stimulus relevance and also its probability, the strongest reactions observed in response to task relevant stimuli occurring with low probability. The response-related activities occurred prior to initiation of movements, dependent upon the particular action and its probability. The data suggest at least two different and spatially overlapping subcortical channels responsible for goal-directed behaviour: the one related to stimulus assessment and the other to preparation for motor action.     

Biomechatronics--assisting the impaired motor system

Biomechatronics concerns the interdisciplinary field of interaction with the human neuromuscular-skeletal system with the objective to assist impaired human motor control. In this field technology is developed that integrates neuroscience, robotics, interface and sensor technology, dynamic systems and control theory. The primary issue in this field concerns the concepts of assisting impaired human motor function. The secondary, derived, issue concerns possible methods of interfacing with the human body at all hierarchical levels of the human motor system. The application of motor assist systems may serve several goals: it can take over part of the affected motor control, enable the physiological motor system to perform the desired function or aid in training the impaired physiological system. The progress in these issues are reviewed and their potential implications for assistance of the impaired human motor system are discussed.     

Age-related neural dedifferentiation in the motor system

Recent neuroimaging studies using multi-voxel pattern analysis (MVPA) show that distributed patterns of brain activation elicited by different visual stimuli are less distinctive in older adults than in young adults. However, less is known about the effects of aging on the neural representation of movement. The present study used MVPA to compare the distinctiveness of motor representations in young and older adults. We also investigated the contributions of brain structure to age differences in the distinctiveness of motor representations. We found that neural distinctiveness was reduced in older adults throughout the motor control network. Although aging was also associated with decreased gray matter volume in these regions, age differences in motor distinctiveness remained significant after controlling for gray matter volume. Our results suggest that age-related neural dedifferentiation is not restricted to sensory perception and is instead a more general feature of the aging brain.     

MODEM: a multi-agent hierarchical structure to model the human motor control system

In this study, based on behavioral and neurophysiological facts, a new hierarchical multi-agent architecture is proposed to model the human motor control system. Performance of the proposed structure is investigated by simulating the control of sit to stand movement. To develop the model, concepts of mixture of experts, modular structure, and some aspects of equilibrium point hypothesis were brought together. We have called this architecture MODularized Experts Model (MODEM). Human motor system is modeled at the joint torque level and the role of the muscles has been embedded in the function of the joint compliance characteristics. The input to the motor system, i.e., the central command, is the reciprocal command. At the lower level, there are several experts to generate the central command to control the task according to the details of the movement. The number of experts depends on the task to be performed. At the higher level, a “gate selector” block selects the suitable subordinate expert considering the context of the task. Each expert consists of a main controller and a predictor as well as several auxiliary modules. The main controller of an expert learns to control the performance of a given task by generating appropriate central commands under given conditions and/or constraints. The auxiliary modules of this expert learn to scrutinize the generated central command by the main controller. Auxiliary modules increase their intervention to correct the central command if the movement error is increased due to an external disturbance. Each auxiliary module acts autonomously and can be interpreted as an agent. Each agent is responsible for one joint and, therefore, the number of the agents of each expert is equal to the number of joints. Our results indicate that this architecture is robust against external disturbances, signal-dependent noise in sensory information, and changes in the environment. We also discuss the neurophysiological and behavioral basis of the proposed model (MODEM).