Task-relevant modulation of primary somatosensory cortex suggests a prefrontal-cortical sensory gating system

Increasing evidence suggests that somatosensory information is modulated cortically for task-specific sensory inflow: Several studies report short-term adaptation of representational maps in primary somatosensory cortex (SI) due to attention or induced by task-related motor activity such as handwriting. Recently, it has been hypothesized that the frontal or prefrontal cortex may modulate SI. In order to test this hypothesis, we studied the functional organization of SI while subjects performed the Tower of Hanoi task. This task is known to be related to activation of frontal or prefrontal areas. The functional organization of SI while performing the Tower of Hanoi task was compared to the organization of SI during performing the same movements but without the Tower of Hanoi task and with rest. Topography of SI was assessed using neuromagnetic source imaging based on tactile stimulation of the first (D1) and fifth digits (D5). Performing the Tower of Hanoi task was accompanied by plastic changes in SI as indicated by significant shifts in the cortical representations of D1 and D5: They moved further apart during the Tower of Hanoi task compared to the control task containing the same movements but without the cognitive characteristic. Thus, we conclude that SI maps undergo dynamic modulation depending on motor tasks with different cognitive demands. The results suggest that this short-term plasticity may be regulated by a prefrontal-cortical sensory gating system.     

Task-specific plasticity of somatosensory cortex in patients with writer's cramp

Focal dystonias such as writer's cramp are characterized by muscular cramps that accompany the execution of specific motor tasks. Until now, the pathophysiology of focal dystonia remains incompletely understood. Recent studies suggest that the development of writer's cramp is related to abnormal organization of primary somatosensory cortex (SI), which in turn leads to impaired motor function. To explore contributions of SI on mechanisms of task specificity in focal dystonia, we investigated dynamic alterations in the functional organization of SI as well as sensory-motor gating for rest, left- and right-handed writing and brushing in writer's cramp patients and healthy controls. The functional organization of somatosensory cortex was assessed by neuromagnetic source imaging (151 channel whole-head MEG). In accordance with previous reports, distances between cortical representations of thumb and little finger of the affected hand were smaller in patients compared to healthy subjects. However, similar to healthy controls, patients showed normal modulation of the functional organization of SI as induced by the execution of different motor tasks. Both in the control subjects and patients, cortical distances between representations of thumb and little finger increased when writing and brushing compared to the resting condition. Although, cramps only occured during writing, no differences in the organization of SI were seen among motor tasks. Our data suggest that despite alterations in the organization of primary somatosensory cortex in writer's cramp, the capability of SI to adapt dynamically to different tasks is not impaired.     

Connectivity exploration with structural equation modeling: an fMRI study of bimanual motor coordination

The present fMRI study explores the connectivity among motor areas in a bimanual coordination task using the analysis framework of structural equation modeling (SEM). During bimanual finger tapping at different frequency ratios, temporal correlations of activations between left/right primary motor cortices (MI), left/right PMdc (caudal dorsal premotor area) and supplementary motor cortex (SMA) were detected and used as inputs to the SEM analysis. SEM was extended from its traditional role as a confirmatory analysis to be used as an exploratory technique to determine the most statistically significant connectivity model given a set of cortical areas based on anatomic constraints. The resultant network exhibits coupling from left MI to right MI, links from both PMs to the two MIs, a negative interaction from left PM to right PM, and functional influence from SMA to right MI and right PM, revealing contributions of these areas to bimanual coordination.     

Morphing the body: illusory feeling of an elongated arm affects somatosensory homunculus

Recent studies suggest that in contrast to traditional views of the body map the topographic representation in primary somatosensory cortex (SI) reflects the perceived rather than the physical aspects of peripheral stimulation. Here, we created a simple illusion of feeling an elongated arm by using the dominance of the visual domain over the tactile sense: employing an artificial hand and arm, which were connected to the body, subjects were given the visual impression that they had an extended arm. Since it is known from animal studies that tactile illusions alter early sensory processing in SI, we expected a modulation of the topography in SI corresponding to this illusion. Behavioral results showed that during the illusion the participants felt that their arm was elongated. Neuromagnetic source imaging of the functional organization in SI revealed that the cortical distance between first (D1) and fifth digit (D5) decreased when subjects felt the arm elongated. Since this modulation was significantly positively correlated with the illusionary feeling of an extended arm, the results suggest an involvement of SI during perceived changes in the size of body parts. We discuss the results as possible top-down modulations of SI by higher order somatosensory areas.     

A comparative fMRI study of cortical representations for thermal painful, vibrotactile, and motor performance tasks.

Cortical activity due to a thermal painful stimulus applied to the right hand was studied in the middle third of the contralateral brain and compared to activations for vibrotactile and motor tasks using the same body part, in nine normal subjects. Cortical activity was demonstrated utilizing multislice echo-planar functional magnetic resonance imaging (fMRI) and a surface coil. The cortical activity was analyzed based upon individual subject activity maps and on group-averaged activity maps. The results show significant differences in activations across the three tasks and the cortical areas studied. The study indicates that fMRI enables examination of cortical networks subserving pain perception at an anatomical detail not available with other brain imaging techniques and shows that this cortical network underlying pain perception shares components with the networks underlying touch perception and motor execution. However, the thermal pain perception network also has components that are unique to this perception. The uniquely activated areas were in the secondary somatosensory region, insula, and posterior cingulate cortex. The posterior cingulate cortex activity was in a region that, in the monkey, receives nociceptive inputs from posterior thalamic medial and lateral nuclei that in turn are targets for spinothalamic terminations. Discrete subdivisions of the primary somatosensory and motor cortical areas were also activated in the thermal pain task, showing region-dependent differences in the extent of overlap with the other two tasks. Within the primary motor cortex, a hand region was preferentially active in the task in which the stimulus was painful heat. In the primary somatosensory cortex most activity in the painful heat task was localized to area 1, where the motor and vibratory task activities were also coincident. The study also indicates that the functional connectivity across multiple cortical regions reorganizes dynamically with each task.     

Fingertip Representation in the Human Somatosensory Cortex: An fMRI Study

Eight right-handed adult humans underwent functional magnetic resonance imaging (fMRI) of their brain while a vibratory stimulus was applied to an individual digit tip (digit 1, 2, or 5) on the right hand. Multislice echoplanar imaging techniques were utilized during digit stimulation to investigate the organization of the human primary somatosensory (SI) cortex, cortical regions located on the upper bank of the Sylvian fissure (SII region), insula, and posterior parietal cortices. Thettest and cluster size analyses were performed to produce cortical activation maps, which exhibited significant regions of interest (ROIs) in all four cortical regions investigated. The frequency of significant ROIs was much higher in SI and the SII region than in the insula and posterior parietal region. Multiple digit representations were observed in the primary somatosensory cortex, corresponding to the four anatomic subdivisions of this cortex (areas 3a, 3b, 1, and 2), suggesting that the organization of the human somatosensory cortex resembles that described in other primates. Overall, there was no simple medial to lateral somatotopic representation in individual subject activity maps. However, the spatial distance between digit 1 and digit 5 cortical representations was the greatest in both SI and the SII region within the group. Statistical analyses of multiple activity parameters showed significant differences between cortical regions and between digits, indicating that vibrotactile activations of the cortex are dependent on both the stimulated digit and cortical region investigated.     

The functional neuroanatomy of coordinated orofacial movements: sparse sampling fMRI of whistling

Whistling serves as a model for a skilful coordinated orofacial movement with sensorimotor integration of auditory and proprioceptive input. The neural substrate of whistling was investigated by sparse sampling functional MRI (fMRI) where the motor task occurred during a silent interval between successive image acquisitions to minimize task-related imaging artefacts. Whistling recruited a symmetrically represented neural network including primary motor and ventral premotor cortex (PMv), SMA, cingulate gyrus, basal ganglia, primary and secondary somatosensory cortex, amygdala, thalamus and cerebellum. A temporal analysis revealed higher activity of left sensory cortex, right PMv and cerebellum during late execution compared to initiation of whistling. Task-related signal changes in right PMv and right paravermal cerebellum were found to correlate with the amplitude of the whistle sound in a separate correlation analysis. The findings emphasize the role of ventral premotor cortex, cerebellum and somatosensory areas as integrators of afferent input within a distributed orofacial sensorimotor network.     

A simultaneous EEG-fMRI study of painful electric stimulation

Together with a detailed behavioral analysis, simultaneous measurement of functional magnetic resonance imaging (fMRI) and electroencephalography (EEG) permits a better elucidation of cortical pain processing. We applied painful electrical stimulation to 6 healthy subjects and acquired fMRI simultaneously with an EEG measurement. The subjects rated various stimulus properties and the individual affective state. Stimulus-correlated BOLD effects were found in the primary and secondary somatosensory areas (SI and SII), the operculum, the insula, the supplementary motor area (SMA proper), the cerebellum, and posterior parts of the anterior cingulate gyrus (ACC). Perceived pain intensity was positively correlated with activation in these areas. Higher unpleasantness rating was associated with suppression of activity in areas known to be involved in stimulus categorization and representation (ventral premotor cortex, PCC, parietal operculum, insula) and enhanced activation in areas initiating, propagating, and executing motor reactions (ACC, SMA proper, cerebellum, primary motor cortex). Concordant dipole localizations in SI and ACC were modeled. Using the dipole strength in SI, the network was restricted to SI. The BOLD signal change in ACC was positively correlated to the individual dipole strength of the source in ACC thus revealing a close relationship of BOLD signal and possibly underlying neuronal electrical activity in SI and the ACC. The BOLD signal change decreased in SI over time. Dipole strength of the ACC source decreased over the experiment and increased during the stimulation block suggesting sensitization and habituation effects in these areas.     

Measuring interregional functional connectivity using coherence and partial coherence analyses of fMRI data

Understanding functional connectivity within the brain is crucial to understanding neural function; even the simplest cognitive operations are supported by highly distributed neural circuits. We developed a novel method to measure task-related functional interactions between neural regions by applying coherence and partial coherence analyses to functional magnetic resonance imaging (fMRI) data. Coherence and partial coherence are spectral measures that estimate the linear time-invariant (LTI) relationship between time series. They can be used to generate maps of task-specific connectivity associated with seed regions of interest (ROIs). These maps may then be compared across tasks, revealing nodes with task-related changes of connectivity to the seed ROI. To validate the method, we applied it to an event-related fMRI data set acquired while subjects performed two sequence tapping tasks, one of which required more bimanual coordination. Areas showing increased functional connectivity with both tasks were the same as those showing increased activity. Furthermore, though there were no significant differences in mean activity between the two tasks, significant increases in interhemispheric coherence were found between the primary motor (M1) and premotor (PM) regions for the task requiring more bimanual coordination. This increase in interhemispheric connectivity is supported by other brain imaging techniques as well as patient studies.     

Cortical mechanisms for acquisition and performance of bimanual motor sequences

We used functional magnetic resonance imaging to investigate the cortical mechanisms contributing to the acquisition and performance of a complex, bimanual motor sequence. To that aim, five subjects were trained on a difficult, asymmetrical finger opposition task. Their performance rate almost doubled in the course of training and approached the performance rate in an untrained, symmetrical finger opposition task. Before training, performance of the asymmetrical sequence was associated with activity in M1, premotor cortex, supplementary motor cortex, and parietal cortex. After training, performance of the asymmetrical sequence was associated mainly with activity in M1, and little activity outside M1 remained. The latter pattern of cortical activation resembled that observed during the execution of symmetrical sequences, which was unaffected by practice with the asymmetrical sequence. The activation pattern obtained with the symmetrical bimanual sequence was indistinguishable from the combined activation measured in contralateral hemispheres during unimanual control sequences. The data indicate that cortical regions previously implicated in the acquisition of difficult unimanual motor sequences also contribute to the acquisition of asymmetrical bimanual sequences. We found no evidence for an expansion of activity in M1 after acquisition of the asymmetrical sequence (while this has been reported after acquisition of unimanual sequences). In the context of existing literature, the data suggest that the acquisition of unimanual and bimanual motor sequences may rely on similar cortical mechanisms, but that the formation of long-term, procedural memories for the two types of sequences might at least in part depend on different mechanisms.     

Evidence for premotor cortex activity during dynamic visuospatial imagery from single-trial functional magnetic resonance imaging and event-related slow cortical potentials

A strong correspondence has been repeatedly observed between actually performed and mentally imagined object rotation. This suggests an overlap in the brain regions involved in these processes. Functional neuroimaging studies have consistently revealed parietal and occipital cortex activity during dynamic visuospatial imagery. However, results concerning the involvement of higher-order cortical motor areas have been less consistent. We investigated if and when premotor structures are active during processing of a three-dimensional cube comparison task that requires dynamic visuospatial imagery. In order to achieve a good temporal and spatial resolution, single-trial functional magnetic resonance imaging (fMRI) and scalp-recorded event-related slow cortical potentials (SCPs) were recorded from the same subjects in two separate measurement sessions. In order to reduce inter-subject variability in brain activity due to individual differences, only male subjects (n = 13) with high task-specific ability were investigated. Functional MRI revealed consistent bilateral activity in the occipital (Brodmann area BA18/19) and parietal cortex (BA7), in lateral and medial premotor areas (BA6), the dorsolateral prefrontal cortex (BA9), and the anterior insular cortex. The time-course of SCPs indicated that task-related activity in these areas commenced approximately 550-650 ms after stimulus presentation and persisted until task completion. These results provide strong and consistent evidence that the human premotor cortex is involved in dynamic visuospatial imagery.     

Task-dependent modulations of cortical oscillatory activity in human subjects during a bimanual precision grip task

Oscillations are a widespread feature of normal brain activity and have been reported at a variety of different frequencies in different neuronal systems. The demonstration that oscillatory activity is present in motor command signals has prompted renewed interest in the possible functions of synchronous oscillatory activity within the primate sensorimotor system. In the current study, we investigated task-dependent modulations in coupling between sensorimotor cortical oscillators during a bimanual precision grip task. The task required a hold-ramp-hold pattern of grip force to be exerted on a compliant object with the dominant right hand, while maintaining a steady grip with the nondominant hand. We found significant task-related modulation of 15- to 30-Hz coherence between magnetoencephalographic (MEG) activity recorded from the left sensorimotor cortex and electromyographic (EMG) activity in hand muscles on the right side. This coherence was maximal during steady hold, but disappeared during the ramp movements. Interestingly coherence between the right sensorimotor MEG and left-hand EMG showed a similar, although less deeply modulated, task-related pattern, even though this hand was maintaining a simple steady grip. No significant ipsilateral MEG-EMG coherence was observed in the 15- to 30-Hz passband for either hand. These results suggest that the cortical oscillators in the two sensorimotor cortices are independent to some degree but that they may share a common mechanism that attenuates the cortical power in both hemispheres in the 15- to 30-Hz range during movements of one hand. The results are consistent with the hypothesis that oscillatory activity in the motor system is important in resetting the descending motor commands needed for changes in motor state, such as those that occur in the transition from movement to steady grip.     

Shared networks for auditory and motor processing in professional pianists: evidence from fMRI conjunction

To investigate cortical auditory and motor coupling in professional musicians, we compared the functional magnetic resonance imaging (fMRI) activity of seven pianists to seven non-musicians utilizing a passive task paradigm established in a previous learning study. The tasks involved either passively listening to short piano melodies or pressing keys on a mute MRI-compliant piano keyboard. Both groups were matched with respect to age and gender, and did not exhibit any overt performance differences in the keypressing task. The professional pianists showed increased activity compared to the non-musicians in a distributed cortical network during both the acoustic and the mute motion-related task. A conjunction analysis revealed a distinct musicianship-specific network being co-activated during either task type, indicating areas involved in auditory-sensorimotor integration. This network is comprised of dorsolateral and inferior frontal cortex (including Broca's area), the superior temporal gyrus (Wernicke's area), the supramarginal gyrus, and supplementary motor and premotor areas.     

Information processing in human parieto-frontal circuits during goal-directed bimanual movements

It is known that, in macaques, movements guided by somatosensory information engage anterior parietal and posterior precentral regions. Movements performed with both visual and somatosensory feedback additionally activate posterior parietal and anterior precentral areas. It remains unclear whether the human parieto-frontal circuits exhibit a similar functional organization. Here, we employed a directional interference task requiring a continuous update of sensory information for the on-line control of movement direction, while brain activity was measured by functional magnetic resonance imaging (fMRI). Directional interference arises when bimanual movements occur along different directions in joint space. Under these circumstances, the presence of visual information does not substantially alter performance, such that we could vary the amount and type of sensory information used during on-line guidance of goal-directed movements without affecting motor output. Our results confirmed that in humans, as in macaques, movements guided by somatosensory information engages anterior parietal and posterior precentral regions, while movements performed with both visual and somatosensory information activate posterior parietal and anterior precentral areas. We provide novel evidence on how the interaction of specific portions of the dorsal parietal and precentral cortex in the right hemisphere might generate spatial representations by integrating different sensory modalities during goal-directed movements.     

Three-dimensional locations and boundaries of motor and premotor cortices as defined by functional brain imaging: a meta-analysis

The mesial premotor cortex (pre-supplementary motor area and supplementary motor area proper), lateral premotor cortex (dorsal premotor cortex and ventral premotor cortex), and primary sensorimotor cortex (primary motor cortex and primary somatosensory cortex) have been identified as key cortical areas for sensorimotor function. However, the three-dimensional (3-D) anatomic boundaries between these regions remain unclear. In order to clarify the locations and boundaries for these six sensorimotor regions, we surveyed 126 articles describing pre-supplementary motor area, supplementary motor area proper, dorsal premotor cortex, ventral premotor cortex, primary motor cortex, and primary somatosensory cortex. Using strict inclusion criteria, we recorded the reported normalized stereotaxic coordinates (Talairach and Tournoux or MNI) from each experiment. We then computed the probability distributions describing the likelihood of activation, and characterized the shape, extent, and area of each sensorimotor region in 3-D. Additionally, we evaluated the nature of the overlap between the six sensorimotor regions. Using the findings from this meta-analysis, along with suggestions and guidelines of previous researchers, we developed the Human Motor Area Template (HMAT) that can be used for ROI analysis. HMAT is available through e-mail from the corresponding author.     

Cortical networks subserving upper limb movements in primates

In all primates, the cortical control of hand and arm movements is initiated and controlled by a network of cortical regions including primary motor cortex (M1), premotor cortex (PMC), and posterior parietal cortex (PPC). These interconnected regions are influenced by inputs from especially visual and somatosensory cortical areas, and prefrontal cortex. Here we discuss recent evidence showing M1, PMC, and PPC can be subdivided into a number of functional zones or domains, including several that participate in guiding and controlling hand and arm movements. Functional zones can be defined by the movement sequences evoked by microstimulation within them, and functional zones related to the same type of movement in all three cortical regions are interconnected. The inactivation of a functional zone in each of the regions has a different impact on motor behavior. Finally, there is considerable plasticity within the networks so that behavioral recoveries can occur after damage to functional zones within a network.     

Cortical activity in multiple motor areas during sequential finger movements: an application of independent component analysis

Multiple cortical regions such as the supplementary motor area (SMA), premotor cortex (PM), and primary motor cortex (M1) are involved in the sequential execution of hand movements, but it is unclear how these areas collaborate in the preparation and execution of ipsilateral and contralateral hand movements. In this study, we used right-handed subjects to examine the spatial distribution and temporal profiles of motor-related activity during visually cued sequential finger movements by applying independent component analysis (ICA) to event-related functional magnetic resonance imaging (fMRI) signals. The particular merit of the ICA method is that it allows brain activity in individual subjects to be elucidated without making a priori assumptions about the anatomical areas that are activated or the temporal profile of activity. By applying ICA, we found that (1) the SMA contributed to both the preparation and execution of movements of the right and left hand; (2) the left M1 and dorsal premotor cortex (PMd) contributed to both the preparation and execution of movements of the right and left hand, whereas the right M1 and PMd contributed mainly to the execution of movements of the left hand; (3) pre-SMA areas were activated in some subjects in concert with the posterior parietal and prefrontal cortex; and (4) fMRI signals over superficial cortical draining veins could be distinguished from cortical activation. We suggest that ICA is useful for categorizing distributed task-related activities in individual subjects into several spatially independent activities that represent functional units in motor control.     

Functional mapping of cortical areas with optical imaging

Sensory areas in mammalian cortex compute sensory inputs of different modalities in order to perceive the environment. Much is known about the anatomical pattern of inter-laminar connections, which form the basis of the computational process. Nevertheless, less is known about the functional relevance of these wiring patterns. We used intrinsic optical signals (IOSs) in vitro to investigate functional properties of inter-laminar connections in cortical brain slices of rat sensory cortex. By electrical stimulation in layer VI, a columnar-shaped IOS in all cortical areas was found. We detected different laminar patterns of activation in different cortical areas. In primary sensory areas, like primary visual cortex and primary somatosensory cortex, the peak intensity of IOSs occurred in layer IV, which receives the main thalamic input. In secondary sensory areas, like the secondary visual cortex or the secondary somatosensory cortex, the maximum of IOSs amplitude was shifted to layer II/III. In motor areas, IOS peak amplitude is located in layer II/III. In the hind limb area, considered as amalgam between sensory and motor function, a mixture of the activity patterns observed in primary sensory and a motor area occurred with a peak amplitude in layers II and IV. At different stimulation sites within one cortical area, the shape of columnar IOSs remained very similar, reflecting a canonical architecture of functional micro-circuitry. We conclude that both primary and secondary sensory cortical areas display their characteristic functional activation pattern, regardless of their sensory modalities.     

Frontal regions involved in learning of motor skill--A functional NIRS study

To investigate cerebral mechanisms underlying learning of motor skill, we assessed serial changes of cortical activation patterns during a pursuit rotor (PR) task in 18 right-handed, healthy subjects using a functional near-infrared spectroscopy (fNIRS) system. Subjects performed the task with the right hand for 30 s alternated with 30-s rest for 8 repetitions (cycle1 to 8). Gains in motor skill were evaluated by time for keeping the stylus on the target (max 30 s), surface EMG patterns and trajectories of the arm. Performance improved with repetitions of the task cycles (12.9/17.1/19.3/20.0/21.1/22.2/23.6/23.9 s on average) and reached plateau at the 7th cycle. Reciprocal EMG patterns and steady trajectories were associated with acquisition of the motor skill. Task-related increases of oxygenated hemoglobin (oxyHb) were observed in the channels covering the sensorimotor cortex (SMC), premotor and prefrontal regions. There were also task-related decreases of deoxygenated hemoglobin (deoxyHb) in these areas although the changes were smaller compared with those of oxyHb. The center of task-related increases of oxyHb was initially located in the presupplementary motor area (preSMA) and shifted caudally to the supplementary motor area (SMA) with cycle repetitions. The ratios of oxyHb changes in preSMA to SMA significantly decreased with task repetitions. DeoxyHb changes confirmed the activation patterns. These data suggest that preSMA plays an important role in the early phase of motor learning while the SMA might be more involved in the late learning phase of the motor skill.     

Brain mechanisms for preparing increasingly complex sensory to motor transformations

Movements made in response to sensory cues require the brain to transform sensory information into an appropriate motor output. Sensorimotor mappings used in daily life range from direct or "standard" to highly complex. In "nonstandard" sensorimotor tasks, the visual stimulus guiding an action is often not the target of the action. A common example of such a nonstandard mapping is the use of a computer mouse on a horizontal surface to guide an object visible on a vertical monitor. The present study used event-related BOLD fMRI to examine how patterns of brain activity vary as sensorimotor mappings become progressively more complicated. We observed significantly different patterns of cortical activity depending on the level of dissociation between a sensory input and a required motor response. Our results suggest the presence of a functional network generally involved in performing the type of nonstandard sensorimotor tasks examined. This putative network includes regions of the primary motor cortex, medial motor areas, the superior parietal lobule (SPL), and the lateral premotor cortex. The extent of activity in active areas varied depending on the characteristics of the particular sensorimotor mapping used in performing a task. Furthermore, in addition to this putative network, specific task-related areas of activity were observed.