FMRI supports the sensorimotor theory of motor resonance

The neural mechanisms mediating the activation of the motor system during action observation, also known as motor resonance, are of major interest to the field of motor control. It has been proposed that motor resonance develops in infants through Hebbian plasticity of pathways connecting sensory and motor regions that fire simultaneously during imitation or self movement observation. A fundamental problem when testing this theory in adults is that most experimental paradigms involve actions that have been overpracticed throughout life. Here, we directly tested the sensorimotor theory of motor resonance by creating new visuomotor representations using abstract stimuli (motor symbols) and identifying the neural networks recruited through fMRI. We predicted that the network recruited during action observation and execution would overlap with that recruited during observation of new motor symbols. Our results indicate that a network consisting of premotor and posterior parietal cortex, the supplementary motor area, the inferior frontal gyrus and cerebellum was activated both by new motor symbols and by direct observation of the corresponding action. This tight spatial overlap underscores the importance of sensorimotor learning for motor resonance and further indicates that the physical characteristics of the perceived stimulus are irrelevant to the evoked response in the observer.     

Phase relationships of cerebral cortex potentials in the rabbit during the execution of motor responses

EEG waves phase relations in the sensorimotor and visual cortical areas were studied in 12 rabbits before and during a motor reaction in response to light stimulation. Phase relations in the background activity were characterized by a considerable dispersion (from 26 to 45 degrees). Light stimulation increased the quantity of synphasic EEG oscillations in adjacent cortical points and stabilized the phase shift between EEG waves in the sensorimotor and visual cortical areas. Motor reactions of rabbits to light occurred when theta-rhythm with the most constant phase shift was observed in the EEG of these areas.     

Multivariate EEG spectral analysis evidences the functional link between motor and visual cortex during integrative sensorimotor tasks

The identification of the networks connecting brain areas and the understanding of their role in executing complex tasks is a crucial issue in cognitive neuroscience. In this study, specific visuomotor tasks were devised to reveal the functional network underlying the cooperation process between visual and motor regions. Electroencephalography (EEG) data were recorded from twelve healthy subjects during a combined visuomotor task, which integrated precise grip motor commands with sensory visual feedback (VM). This condition was compared with control tasks involving pure motor action (M), pure visual perception (V) and visuomotor performance without feedback (V + M). Multivariate parametric cross-spectral analysis was applied to ten EEG derivations in each subject to assess changes in the oscillatory activity of the involved cortical regions and quantify their coupling. Spectral decomposition was applied to precisely and objectively determine the power associated with each oscillatory component of the spectrum, while surrogate data analysis was performed to assess the statistical significance of estimated coherence values. A significant decrease of the alpha and/or beta power in EEG spectra with respect to rest values was assumed as indicative of specific cortical area activation during task execution. Indeed alpha band coherence increased in proximity of task-involved areas, while it was suppressed or remained unchanged in other regions, suggesting the activation of a specific network for each task. According to our coherence analysis, a direct link between visual and motor areas was activated during V + M and VM tasks. The effect of visual feedback was evident in the beta band, where the increase of coherence was observed only during the VM task. Multivariate analysis suggested the presence of a functional link between motor and visual cortex subserving sensorimotor integration. Furthermore, network activation was related to the sum of single task (M and V) local effects in the alpha band, and to the presence of visual feedback in the beta band.     

The golden beauty: brain response to classical and renaissance sculptures

Is there an objective, biological basis for the experience of beauty in art? Or is aesthetic experience entirely subjective? Using fMRI technique, we addressed this question by presenting viewers, naïve to art criticism, with images of masterpieces of Classical and Renaissance sculpture. Employing proportion as the independent variable, we produced two sets of stimuli: one composed of images of original sculptures; the other of a modified version of the same images. The stimuli were presented in three conditions: observation, aesthetic judgment, and proportion judgment. In the observation condition, the viewers were required to observe the images with the same mind-set as if they were in a museum. In the other two conditions they were required to give an aesthetic or proportion judgment on the same images. Two types of analyses were carried out: one which contrasted brain response to the canonical and the modified sculptures, and one which contrasted beautiful vs. ugly sculptures as judged by each volunteer. The most striking result was that the observation of original sculptures, relative to the modified ones, produced activation of the right insula as well as of some lateral and medial cortical areas (lateral occipital gyrus, precuneus and prefrontal areas). The activation of the insula was particularly strong during the observation condition. Most interestingly, when volunteers were required to give an overt aesthetic judgment, the images judged as beautiful selectively activated the right amygdala, relative to those judged as ugly. We conclude that, in observers naïve to art criticism, the sense of beauty is mediated by two non-mutually exclusive processes: one based on a joint activation of sets of cortical neurons, triggered by parameters intrinsic to the stimuli, and the insula (objective beauty); the other based on the activation of the amygdala, driven by one''s own emotional experiences (subjective beauty).     

Finding the beat: a neural perspective across humans and non-human primates

Humans possess an ability to perceive and synchronize movements to the beat in music (‘beat perception and synchronization’), and recent neuroscientific data have offered new insights into this beat-finding capacity at multiple neural levels. Here, we review and compare behavioural and neural data on temporal and sequential processing during beat perception and entrainment tasks in macaques (including direct neural recording and local field potential (LFP)) and humans (including fMRI, EEG and MEG). These abilities rest upon a distributed set of circuits that include the motor cortico-basal-ganglia–thalamo-cortical (mCBGT) circuit, where the supplementary motor cortex (SMA) and the putamen are critical cortical and subcortical nodes, respectively. In addition, a cortical loop between motor and auditory areas, connected through delta and beta oscillatory activity, is deeply involved in these behaviours, with motor regions providing the predictive timing needed for the perception of, and entrainment to, musical rhythms. The neural discharge rate and the LFP oscillatory activity in the gamma- and beta-bands in the putamen and SMA of monkeys are tuned to the duration of intervals produced during a beat synchronization–continuation task (SCT). Hence, the tempo during beat synchronization is represented by different interval-tuned cells that are activated depending on the produced interval. In addition, cells in these areas are tuned to the serial-order elements of the SCT. Thus, the underpinnings of beat synchronization are intrinsically linked to the dynamics of cell populations tuned for duration and serial order throughout the mCBGT. We suggest that a cross-species comparison of behaviours and the neural circuits supporting them sets the stage for a new generation of neurally grounded computational models for beat perception and synchronization.     

Bioelectric brain activity during visual perception of verbalized and nonverbalized stimuli in seven-to eight-year-old schoolchildren

Neurophysiological mechanisms of visual perception of verbalized and nonverbalized stimuli have been studied in girls (n = 89) and boys (n = 109) aged seven to eight years. It has been shown that, in children of this age, neurophysiological mechanisms of the visual perception system during the selection of verbalized and nonverbalized stimuli have similar organizations of functional rearrangements and are characterized by the general involvement of cortical areas and by the lack of clear specialization of the cerebral hemispheres. However, the choice of nonverbalized visual stimuli is characterized by a more pronounced generalization of the functional interaction between cortical areas and by the increased spectral power of the EEG’s high-frequency components in anterior associative areas. The increased spatial synchronization in the EEG θ- and β bands in the frontal areas emphasizes the contribution of these structures to the analysis and processing of visual stimuli at this stage of development. Differences in the neurophysiological mechanisms of visual perception in boys and girls have been detected. Spatial and temporal organizations of bioelectric activity (BEA) of the brain in girls performing visual tasks is characterized by a stronger and more varied ipsi- and contralateral statistical relationships in the fronto-occipital direction and displacement of interaction centers to the left hemisphere. In boys perceiving verbalized and nonverbalized visual stimuli, a greater contribution of posterocentral cortical areas has been observed. The detected differences are considered to reflect a greater maturity of identification mechanisms in girls aged seven to eight years as compared to boys.     

Infants’ Somatotopic Neural Responses to Seeing Human Actions: I’ve Got You under My Skin

Human infants rapidly learn new skills and customs via imitation, but the neural linkages between action perception and production are not well understood. Neuroscience studies in adults suggest that a key component of imitation–identifying the corresponding body part used in the acts of self and other–has an organized neural signature. In adults, perceiving someone using a specific body part (e.g., hand vs. foot) is associated with activation of the corresponding area of the sensory and/or motor strip in the observer’s brain–a phenomenon called neural somatotopy. Here we examine whether preverbal infants also exhibit somatotopic neural responses during the observation of others’ actions. 14-month-old infants were randomly assigned to watch an adult reach towards and touch an object using either her hand or her foot. The scalp electroencephalogram (EEG) was recorded and event-related changes in the sensorimotor mu rhythm were analyzed. Mu rhythm desynchronization was greater over hand areas of sensorimotor cortex during observation of hand actions and was greater over the foot area for observation of foot actions. This provides the first evidence that infants’ observation of someone else using a particular body part activates the corresponding areas of sensorimotor cortex. We hypothesize that this somatotopic organization in the developing brain supports imitation and cultural learning. The findings connect developmental cognitive neuroscience, adult neuroscience, action representation, and behavioral imitation.     

Motor polarization dominance and "animal hypnosis"

Two kinds of dominanta were simultaneously formed under conditions of chronic experiments in rabbits. The motor polarization dominanta was formed under exposure of the right sensorimotor cortex of an animal to direct anodic current, and the state of "animal hypnosis" (the second dominanta) was induced. Animal behavior and electrophysiological characteristics were recorded. It was shown that the "animal hypnosis" induced at the optimum of the right motor polarization dominanta inhibited the motor reaction of the "dominant" extremity to testing stimuli. After the "animal hypnosis session, exposure of the right sensorimotor cortex to anodic current produced the latent excitation focus, which did not reach the level of summation. Two days later, exposure to testing stimuli developed the latent foci at first in the right cortex and then in subcortical structures. In the course of recovery of the motor polarization dominanta and its further change for the state characteristic of the "animal hypnosis", the patterns of cortical EEG coherence in the delta range typical of each kind of dominanta alternated in parallel with the time course of state changes.     

Complexity of Motor Sequences and Cortical Reorganization in Parkinson's Disease: A Functional MRI Study

Motor impairment is the most relevant clinical feature in Parkinson''s disease (PD). Functional imaging studies on motor impairment in PD have revealed changes in the cortical motor circuits, with particular involvement of the fronto-striatal network. The aim of this study was to assess brain activations during the performance of three different motor exercises, characterized by progressive complexity, using a functional fMRI multiple block paradigm, in PD patients and matched control subjects. Unlike from single-task comparisons, multi-task comparisons between similar exercises allowed to analyse brain areas involved in motor complexity planning and execution. Our results showed that in the single-task comparisons the involvement of primary and secondary motor areas was observed, consistent with previous findings based on similar paradigms. Most notably, in the multi-task comparisons a greater activation of supplementary motor area and posterior parietal cortex in PD patients, compared with controls, was observed. Furthermore, PD patients, compared with controls, had a lower activation of the basal ganglia and limbic structures, presumably leading to the impairment in the higher levels of motor control, including complexity planning and execution. The findings suggest that in PD patients occur both compensatory mechanisms and loss of efficiency and provide further insight into the pathophysiological role of distinct cortical and subcortical areas in motor dysfunction.     

Effect of stimulation of field CA3 in the dorsal hippocampus on the motor polarization dominant in rabbits

The influence was studied of the stimulation of the CA3 field of the dorsal hippocampus on the course of motor polarization dominant created by the action of the direct current on the rabbit's cortical sensorimotor area. It is shown that hippocampus stimulation by 1 mA current (0.5 ms, 100 Hz, 0.2 s) against the background of the dominant optimum elicits its inhibition. It is manifested in depression of the motor "dominant" reaction of the forelimb to testing stimuli and in abolition of coherent connections of theta-range electrical activity of the sensorimotor cortex and CA3 field of the dorsal hippocampus. On the contrary, the hippocampus stimulation by a weak current (30-50 mcA, 0.5 ms, 30 Hz, 0.2 s) during optimum dominant reinforces it, eliciting a movement of the "dominant" limb. Against the background of an unstable dominant it provides for its activation and stabilization and recovers the dominant in the following days during its extinction.     

The time course of action and action-word comprehension in the human brain as revealed by neurophysiology.

Numerous previous neuroimaging studies suggest an involvement of cortical motor areas not only in action execution but also in action recognition and understanding. Motor areas of the human brain have also been found to activate during the processing of written and spoken action-related words and sentences. Even more strikingly, stimuli referring to different bodily effectors produced specific somatotopic activation patterns in the motor areas. However, metabolic neuroimaging results can be ambiguous with respect to the processing stage they reflect. This is a serious limitation when hypotheses concerning linguistic processes are tested, since in this case it is usually crucial to distinguish early lexico-semantic processing from strategic effects or mental imagery that may follow lexico-semantic information access. Timing information is therefore pivotal to determine the functional significance of motor areas in action recognition and action-word comprehension. Here, we review attempts to reveal the time course of these processes using neurophysiological methods (EEG, MEG and TMS), in visual and auditory domains. We will highlight the importance of the choice of appropriate paradigms in combination with the corresponding method for the extraction of timing information. The findings will be discussed in the general context of putative brain mechanisms of word and object recognition.     

Definitions of state variables and state space for brain-computer interface

Neocortical state variables are defined and evaluated at three levels: microscopic using multiple spike activity (MSA), mesoscopic using local field potentials (LFP) and electrocorticograms (ECoG), and macroscopic using electroencephalograms (EEG) and brain imaging. Transactions between levels occur in all areas of cortex, upwardly by integration (abstraction, generalization) and downwardly by differentiation (speciation). The levels are joined by circular causality: microscopic activity upwardly creates mesoscopic order parameters, which downwardly constrain the microscopic activity that creates them. Integration dominates in sensory cortices. Microscopic activity evoked by receptor input in sensation induces emergence of mesoscopic activity in perception, followed by integration of perceptual activity into macroscopic activity in concept formation. The reverse process dominates in motor cortices, where the macroscopic activity embodying the concepts supports predictions of future states as goals. These macroscopic states are conceived to order mesoscopic activity in patterns that constitute plans for actions to achieve the goals. These planning patterns are conceived to provide frames in which the microscopic activity evolves in trajectories that adapted to the immediate environmental conditions detected by new stimuli. This circular sequence forms the action-perception cycle. Its upward limb is understood through correlation of sensory cortical activity with behavior. Now brain-machine interfaces (BMI) offer a means to understand the downward sequence through correlation of behavior with motor cortical activity, beginning with macroscopic goal states and concluding with recording of microscopic MSA trajectories that operate neuroprostheses. Part 1 develops a hypothesis that describes qualitatively the neurodynamics that supports the action-perception cycle and derivative reflex arc. Part 2 describes episodic, “cinematographic” spatial pattern formation and predicts some properties of the macroscopic and mesoscopic frames by which the embedded trajectories of the microscopic activity of cortical sensorimotor neurons might be organized and controlled. URL: http://sulcus.berkeley.edu     

Recognition of fragmented images and mechanisms of memory

Analysis of the topography and parameters of event-related potentials (ERPs) recorded during the presentation of incomplete images with different fragmentation aided in study of the role of different cortical zones and the order of their involvement in the recognition process. The role of the frontal cortical areas at different stages of perception of fragmented images was established. The differences in the ERPs induced by recognized and unrecognized stimuli in the frontal and frontal-temporal derivations in the interval 30–83 ms were associated with the appearance of early positivity in response to recognized images and development of early negativity in response to unrecognized stimuli. The N300 component associated with recognition was stronger in these cortical zones during identification of images. A late positive complex appeared in the frontal areas earlier than in other areas. Involvement of the caudal visual areas in the recognition process was reflected by enhancement of the components P100, P250, and N400. Our results suggest that the frontal areas play the main role in the recognition of fragmented images because they are the structures that organize extraction of traces from long-term modality-specific memory using a system of afferent and efferent links and determine the strategy of information analysis necessary for the solution of a given task.     

Persistence of Cortical Sensory Processing during Absence Seizures in Human and an Animal Model: Evidence from EEG and Intracellular Recordings

Absence seizures are caused by brief periods of abnormal synchronized oscillations in the thalamocortical loops, resulting in widespread spike-and-wave discharges (SWDs) in the electroencephalogram (EEG). SWDs are concomitant with a complete or partial impairment of consciousness, notably expressed by an interruption of ongoing behaviour together with a lack of conscious perception of external stimuli. It is largely considered that the paroxysmal synchronizations during the epileptic episode transiently render the thalamocortical system incapable of transmitting primary sensory information to the cortex. Here, we examined in young patients and in the Genetic Absence Epilepsy Rats from Strasbourg (GAERS), a well-established genetic model of absence epilepsy, how sensory inputs are processed in the related cortical areas during SWDs. In epileptic patients, visual event-related potentials (ERPs) were still present in the occipital EEG when the stimuli were delivered during seizures, with a significant increase in amplitude compared to interictal periods and a decrease in latency compared to that measured from non-epileptic subjects. Using simultaneous in vivo EEG and intracellular recordings from the primary somatosensory cortex of GAERS and non-epileptic rats, we found that ERPs and firing responses of related pyramidal neurons to whisker deflection were not significantly modified during SWDs. However, the intracellular subthreshold synaptic responses in somatosensory cortical neurons during seizures had larger amplitude compared to quiescent situations. These convergent findings from human patients and a rodent genetic model show the persistence of cortical responses to sensory stimulations during SWDs, indicating that the brain can still process external stimuli during absence seizures. They also demonstrate that the disruption of conscious perception during absences is not due to an obliteration of information transfer in the thalamocortical system. The possible mechanisms rendering the cortical operation ineffective for conscious perception are discussed, but their definite elucidation will require further investigations.     

The role of premotor cortex in speech perception: evidence from fMRI and rTMS.

This article discusses recent functional magnetic resonance imaging (fMRI) and repetitive Transcranial Magnetic Stimulation (rTMS) data that suggest a direct involvement of premotor cortical areas in speech perception. These new data map well onto psychological theories advocating an active role of motor structures in the perception of speech sounds. It is proposed that the perception of speech is enabled--at least in part--by a process that simulates speech production.     

The mechanism of action of a reinforcing stimulus]

Experiments on alert non-immobilized rabbits revealed that electrical cutaneous stimulation of a limb, used as a reinforcing agent in elaboration of a conditioned reflex to photic flashes, weakened slow polyrhythmic oscillations of background EEG and late components of evoked potentials in the visual cortex to photic flashes. Against this background, the connection between slow potentials and spike activity in both the visual and sensorimotor cortical areas considerably diminished. During EEG activation, induced by the reinforcing stimulus, inhibitory pauses and post-inhibitory activation in the firing of the neocortical units weakened and protracted, ordered spike activity appeared. The data obtained are in agreement with the hypothesis that weakening of the recurrent inhibition system is one of the basic mechanisms in the action of the reinforcing stimulus in conditioning.     

Evaluation of EEG Oscillatory Patterns and Cognitive Process during Simple and Compound Limb Motor Imagery

Motor imagery (MI), sharing similar neural representations to motor execution, is regarded as a window to investigate the cognitive motor processes. However, in comparison to simple limb motor imagery, significantly less work has been reported on brain oscillatory patterns induced by compound limb motor imagery which involves several parts of limbs. This study aims to investigate differences of the electroencephalogram (EEG) patterns as well as cognitive process between simple limb motor imagery and compound limb motor imagery. Ten subjects participated in the experiment involving three tasks of simple limb motor imagery (left hand, right hand, feet) and three tasks of compound limb motor imagery (both hands, left hand combined with right foot, right hand combined with left foot). Simultaneous imagination of different limbs contributes to the activation of larger cortical areas as well as two estimated sources located at corresponding motor areas within beta rhythm. Compared with simple limb motor imagery, compound limb motor imagery presents a network with more effective interactions overlying larger brain regions, additionally shows significantly larger causal flow over sensorimotor areas and larger causal density over both sensorimotor areas and neighboring regions. On the other hand, compound limb motor imagery also shows significantly larger 10–11 Hz alpha desynchronization at occipital areas and central theta synchronization. Furthermore, the phase-locking value (PLV) between central and occipital areas of left/right hand combined with contralateral foot imagery is significantly larger than that of simple limb motor imagery. All these findings imply that there exist apparent intrinsic distinctions of neural mechanism between simple and compound limb motor imagery, which presents a more complex effective connectivity network and may involve a more complex cognitive process during information processing.     

Environmental enrichment modulates cortico-cortical interactions in the mouse

Environmental enrichment (EE) is an experimental protocol based on a complex sensorimotor stimulation that dramatically affects brain development. While it is widely believed that the effects of EE result from the unique combination of different sensory and motor stimuli, it is not known whether and how cortico-cortical interactions are shaped by EE. Since the primary visual cortex (V1) is one of the best characterized targets of EE, we looked for direct cortico-cortical projections impinging on V1, and we identified a direct monosynaptic connection between motor cortex and V1 in the mouse brain. To measure the interactions between these areas under standard and EE rearing conditions, we used simultaneous recordings of local field potentials (LFPs) in awake, freely moving animals. LFP signals were analyzed by using different methods of linear and nonlinear analysis of time series (cross-correlation, mutual information, phase synchronization). We found that EE decreases the level of coupling between the electrical activities of the two cortical regions with respect to the control group. From a functional point of view, our results indicate, for the first time, that an enhanced sensorimotor experience impacts on the brain by affecting the functional crosstalk between different cortical areas.     

Interaction of gustatory and lingual somatosensory perceptions at the cortical level in the human: a functional magnetic resonance imaging study

The present study has investigated interaction at the cortical level in the human between two major components of flavor perception, pure chemical gustatory and lingual somatosensory perception. Twelve subjects participated in a functional magnetic resonance imaging study and tasted six stimuli, applied on the whole tongue, among which four were pure gustatory stimuli (NaCl, aspartame, quinine and HCl, pH 2.4 or 2.2) and two were both taste and lingual somatosensory stimuli, i.e. somato-gustatory stimuli (HCl, pH 1.6 or 1.5, and aluminum potassium sulfate). Functional images were acquired with an echo planar sequence on a 3 T system and were individually processed by correlation with the temporal perception profile. Both sets of stimuli showed activation in the same cortical areas, namely the insula, the rolandic operculum (base of the pre- and post-central gyri), the frontal operculum and the temporal operculum, confirming a wide overlap of taste and lingual somatosensory representations. However, the relative activation across areas and the analysis of co-activated areas across all runs for each set of stimuli allowed discrimination of taste and somatosensory modalities. Factor analysis of correspondences indicated different patterns of activation across the sub-insular and opercular regions, depending on the gustatory or somato-gustatory nature of the stimuli. For gustatory stimuli different activation patterns for the superior and inferior parts of the insula suggested a difference in function between these two insular sub-regions. Furthermore, the left inferior insula was co-activated with the left angular gyrus, a structure involved in semantic processing. In contrast, only somato-gustatory stimuli specifically produced a simultaneous and symmetrical activation of both the left and right rolandic opercula, which include a part of the sensory homunculus dedicated to the tactile representation of oral structures.