A number of studies have demonstrated the involvement of parallel networks in the control of voluntary sequential motor procedures. We sought to determine whether a parallel network organization may be found for complex, sequentially based motor systems that are the product of both voluntary and automatic control processes. Specifically, we sought to determine whether the cortical organizational scheme for voluntary repetitive swallowing in adult humans is characterized by a hierarchical dual-projection model or by modules organized into parallel systems. We utilized functional magnetic resonance imaging (fMRI) to investigate cortical function during normal swallowing tasks in eight healthy human adults. Subjects performed both dry (saliva) and bolus (3 ml/bolus of water) swallows. Activation during swallowing tasks localized to sensorimotor areas (M1, S1, and SMA), S2, premotor cortex, posterior parietal cortex, cingulate gyrus, inferior frontal gyrus, the cerebellum, the insular cortex, auditory cortex, corpus callosum, and the basal ganglia and thalamus. Principal components analysis (PCA) of these regions revealed five functional clusters or modules: (1) sensorimotor areas and cingulate gyrus; (2) inferior frontal gyrus, S2, corpus callosum, basal ganglia and thalamus; (3) premotor cortex and posterior parietal cortex; (4) cerebellum; and (5) insula. Analysis of the functional relationship between these areas demonstrated two parallel loops defined by connections to either the cerebellum or insula and connected through the sensorimotor-cingulate module. Path analysis was performed to test the hypothesis of modules organized into parallel loops versus a hierarchical dual-projection model consisting of two separate, singular hierarchical serial pathways from the sensorimotor cortex or insula to the thalamus. These results support the model of modules organized into parallel loops (P=0.8), but not the hierarchical dual-projection model (P<0.0001). Organization of the control of voluntary repetitive swallowing into two parallel systems may confer the ability to effectively coordinate and integrate this highly complex sequentially based motor behavior.
The issue of how the Euclidean properties of space are represented in the nervous system is a main focus in the study of visual perception, but is equally relevant to motor learning. The goal of our experiments was to investigate how the properties of space guide the remapping of motor coordination. Subjects wore an instrumented data glove that recorded the finger motions. Signals generated by the glove operated a remotely controlled endpoint: a cursor on a computer monitor. The subjects were instructed to execute movements of this endpoint with controlled motions of the fingers. This required inverting a highly redundant map from fingers to cursor motions. We found that 1) after training with visual feedback of the final error (but not of the ongoing cursor motion), subjects learned to map cursor locations into configurations of the fingers; 2) extended practice of movement led to more rectilinear cursor movement, a trend facilitated by training under continuous visual feedback of cursor motions; 3) with practice, subjects reduced motion in the degrees of freedom that did not contribute to the movements of the cursor; 4) with practice, subjects reduced variability of both cursor and hand movements; and 5) the reduction of errors and the increase in linearity generalized beyond the set of movements used for training. These findings suggest that subjects not only learned to produce novel coordinated movement to control the placement of the cursor, but they also developed a representation of the Euclidean space on which hand movements were remapped.
Activation of the primary motor and somatosensory cortices, as well as other sensory-motor areas, occurs with swallowing in normal adults. Differential distribution of cortical activity with different swallowing tasks suggests differential functional organization for different swallowing tasks. Understanding these mechanisms may facilitate improved management and therapeutic intervention for neurogenic and postsurgical dysphagia.
The tongue must move with remarkable speed and precision between multiple orofacial motor behaviors that are executed virtually simultaneously. Our present understanding of these highly integrated relationships has been limited by their complexity. Recent research indicates that the tongue s contribution to complex orofacial movements is much greater than previously thought. The purpose of this paper is to review the neural control of tongue movement and relate it to complex orofacial behaviors. Particular attention will be given to the interaction of tongue movement with respiration and swallowing, because the morbidity and mortality associated with these relationships make this a primary focus of many current investigations. This review will begin with a discussion of peripheral tongue muscle and nerve physiology that will include new data on tongue contractile properties. Other relevant peripheral oral cavity and oropharyngeal neurophysiology will also be discussed. Much of the review will focus on brainstem control of tongue movement and modulation by neurons that control swallowing and respiration, because it is in the brainstem that orofacial motor behaviors sort themselves out from their common peripheral structures. There is abundant evidence indicating that the neural control of protrusive tongue movement by motoneurons in the ventral hypoglossal nucleus is modulated by respiratory neurons that control inspiratory drive. Yet, little is known of hypoglossal motoneuron modulation by neurons controlling swallowing or other complex movements. There is evidence, however, suggesting that functional segregation of respiration and swallowing within the brainstem is reflected in somatotopy within the hypoglossal nucleus. Also, subtle changes in the neural control of tongue movement may signal the transition between respiration and swallowing. The final section of this review will focus on the cortical integration of tongue movement with complex orofacial movements. This section will conclude with a discussion of the functional and clinical significance of cortical control with respect to recent advances in our understanding of the peripheral and brainstem physiology of tongue movement.
Arterial spin labeling (ASL) is a promising non-invasive magnetic resonance imaging (MRI) technique for measuring regional cerebral blood flow (rCBF) or perfusion in vivo. To evaluate the feasibility of ASL as a biomarker for clinical trials, it is important to examine test-retest reproducibility. We investigated both inter-and intra-session reproducibility of perfusion MRI using a pulsed ASL (PASL) sequence PICORE Q2TIPS with an echo-planar imaging (EPI) readout. Structural MRI regions of interest (ROIs) were extracted individually by automated parcellation and segmentation methods using FreeSurfer. These cortical and subcortical ROIs were used to assess regional perfusion stability. Our results indicated regional variability in grey matter rCBF. Although rCBF measurements were characterized by intersubject variation, our results also indicated relatively less within-subject variability estimated as within-subject standard deviation (SD W ) (intersession SD W : 2.0 to 8.8; intrasession SD W : 2.8 to 9.6) and acceptable reliabilities as measured using intraclass correlation coefficient (ICC) (intersession ICC: 0.68 to 0.94; intrasession ICC: 0.66 to 0.95) for regional MRI perfusion measurements using the PICORE Q2TIPS technique. Overall, our findings suggest that PASL is a technique with good within and between session reproducibility. Further reproducibility studies in target populations relevant for specific clinical trials of neurovascular related agents will be important and the present results provide a framework for such assessments.
Prior learning of a motor skill creates motor memories that can facilitate or interfere with learning of new, but related, motor skills. One hypothesis of motor learning posits that for a sensorimotor task with redundant degrees of freedom, the nervous system learns the geometric structure of the task and improves performance by selectively operating within that task space. We tested this hypothesis by examining if transfer of learning between two tasks depends on shared dimensionality between their respective task spaces. Human participants wore a data glove and learned to manipulate a computer cursor by moving their fingers. Separate groups of participants learned two tasks: a prior task that was unique to each group and a criterion task that was common to all groups. We manipulated the mapping between finger motions and cursor positions in the prior task to define task spaces that either shared or did not share the task space dimensions (x-y axes) of the criterion task. We found that if the prior task shared task dimensions with the criterion task, there was an initial facilitation in criterion task performance. However, if the prior task did not share task dimensions with the criterion task, there was prolonged interference in learning the criterion task due to participants finding inefficient task solutions. These results show that the nervous system learns the task space through practice, and that the degree of shared task space dimensionality influences the extent to which prior experience transfers to subsequent learning of related motor skills.
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