Monique Geurts

Brain Activity during Ankle Proprioceptive Stimulation Predicts Balance Performance in Young and Older Adults

Proprioceptive information from the foot/ankle provides important information regarding body sway for balance control, especially in situations where visual information is degraded or absent. Given known increases in catastrophic injury due to falls with older age, understanding the neural basis of proprioceptive processing for balance control is particularly important for older adults. In the present study, we linked neural activity in response to stimulation of key foot proprioceptors (i.e., muscle spindles) with balance ability across the lifespan. Twenty young and 20 older human adults underwent proprioceptive mapping; foot tendon vibration was compared with vibration of a nearby bone in an fMRI environment to determine regions of the brain that were active in response to muscle spindle stimulation. Several body sway metrics were also calculated for the same participants on an eyes-closed balance task. Based on regression analyses, multiple clusters of voxels were identified showing a significant relationship between muscle spindle stimulation-induced neural activity and maximum center of pressure excursion in the anterior–posterior direction. In this case, increased activation was associated with greater balance performance in parietal, frontal, and insular cortical areas, as well as structures within the basal ganglia. These correlated regions were age- and foot-stimulation side-independent and largely localized to right-sided areas of the brain thought to be involved in monitoring stimulus-driven shifts of attention. These findings support the notion that, beyond fundamental peripheral reflex mechanisms, central processing of proprioceptive signals from the foot is critical for balance control.

The neural basis of central proprioceptive processing in older versus younger adults: An important sensory role for right putamen

Our sense of body position and movement independent of vision (i.e., proprioception) relies on muscle spindle feedback and is vital for performing motor acts. In this study, we first sought to elucidate age‐related differences in the central processing of proprioceptive information by stimulating foot muscle spindles and by measuring neural activation with functional magnetic resonance imaging. We found that healthy older adults activated a similar, distributed network of primary somatosensory and secondary‐associative cortical brain regions as young individuals during the vibration‐induced muscle spindle stimulation. A significant decrease in neural activity was also found in a cluster of right putamen voxels for the older age group when compared with the younger age group. Given these differences, we performed two additional analyses within each group that quantified the degree to which age‐dependent activity was related to (1) brain structure and (2) a behavioral measure of proprioceptive ability. Using diffusion tensor imaging, older (but not younger) adults with higher mean fractional anisotropy were found to have increased right putamen neural activity. Age‐dependent right putamen activity seen during tendon vibration was also correlated with a behavioral test of proprioceptive ability measuring ankle joint position sense in both young and old age groups. Partial correlation tests determined that the relationship between elderly joint position sense and neural activity in right putamen was mediated by brain structure, but not vice versa. These results suggest that structural differences within the right putamen are related to reduced activation in the elderly and potentially serve as biomarker of proprioceptive sensibility in older adults. Hum Brain Mapp, 2012.

Brain-Behavior Relationships in Young Traumatic Brain Injury Patients: DTI Metrics are Highly Correlated with Postural Control

Traumatic brain injury (TBI) is a major cause of impairment and functional disability in children and adolescents, including deterioration in fine as well as gross motor skills. The aim of this study was to assess deficits in sensory organization and postural ability in a young group of TBI patients versus controls by using quantitative force‐platform recordings, and to test whether balance deficits are related to variation in structural properties of the motor and sensory white matter pathways. Twelve patients with TBI and 14 controls (aged 8–20 years) performed the Sensory Organisation Test (SOT) protocol of the EquiTest® (Neurocom). All participants were scanned using Diffusion Tensor Imaging (DTI) along with standard anatomical scans. Quantitative comparisons of DTI parameters (fractional anisotropy, axial and radial diffusivity) between TBI patients and controls were performed. Correlations between DTI parameters and SOT balance scores were determined. Findings revealed that the TBI group scored generally lower than the control group on the SOT, indicative of deficits in postural control. In the TBI group, reductions in fractional anisotropy were noted in the cerebellum, posterior thalamic radiation, and corticospinal tract. Degree of white matter deterioration was highly correlated with balance deficits. This study supports the view that DTI is a valuable tool for assessing the integrity of white matter structures and for selectively predicting functional motor deficits in TBI patients. Hum Brain Mapp, 2010.

Brain-behavior relationships in young traumatic brain injury patients: Fractional anisotropy measures are highly correlated with dynamic visuomotor tracking performance

Traumatic brain injury (TBI) patients have a high incidence of eye-hand coordination deficits. Diffuse axonal injury is common in TBI and is presumed to contribute to persistent motor problems. Using Diffusion Tensor Imaging (DTI), this study sought to identify changes in (sensori)motor white matter (WM) pathways/regions in a TBI group during the chronic recovery stage. A secondary objective was to examine the relationship between WM integrity and upper-limb visuomotor tracking performance. A young TBI (n=17) and control (n=14) group performed a dynamic tracking task, characterized by increasing information processing speed and predictive movement control. DTI scans were administered along with standard anatomical scans. The TBI group was found to perform inferior to the control group on the tracking task. Decreased fractional anisotropy was found in the TBI group in dedicated pathways involved in transmission of afferent and efferent information, i.e., corticospinal tract, posterior thalamic radiation, and optic radiation, due to increased diffusivity parallel and perpendicular to axonal fibre direction. This decrease in WM integrity was associated with inferior visuomotor tracking performance. Moreover, discriminant function analysis demonstrated that the model, based on the combined application of DTI and behavioral measures, was the most effective in distinguishing between TBI patients and controls. This study shows that specific eye-hand coordination deficits in a young TBI group are related to microstructural abnormalities in task-specific cerebral WM structures. Measures of white matter integrity are potentially important biomarkers for TBI that may support prognosis of motor deficits.

Bimanual coordination and corpus callosum microstructure in young adults with traumatic brain injury: a diffusion tensor imaging study

Bimanual actions are ubiquitous in daily life. Many coordinated movements of the upper extremities rely on precise timing, which requires efficient interhemispheric communication via the corpus callosum (CC). As the CC in particular is known to be vulnerable to traumatic brain injury (TBI), furthering our understanding of its structure-function association is highly valuable for TBI diagnostics and prognosis. In this study, 21 young adults with TBI and 17 controls performed object manipulation tasks (insertion of pegs with both hands and bilateral daily life activities) and cognitive control tasks (i.e., switching maneuvers during spatially and temporally coupled bimanual circular motions). The structural organization of 7 specific subregions of the CC (prefrontal, premotor/supplementary motor, primary motor, primary sensory, parietal, temporal, and occipital) was subsequently investigated in these subjects with diffusion tensor imaging (DTI). Findings revealed that bimanual coordination was impaired in TBI patients as shown by elevated movement time values during daily life activities, a decreased number of peg insertions, and slower response times during the switching task. Furthermore, the DTI analysis demonstrated a significantly decreased fractional anisotropy and increased radial diffusivity in prefrontal, primary sensory, and parietal regions in TBI patients versus controls. Finally, multiple regression analyses showed evidence of the high specificity of callosal subregions accounting for the variance associated with performance of the different bimanual coordination tasks. Whereas disruption in commissural pathways between occipital areas played a role in performance on the clinical tests of bimanual coordination, deficits in the switching task were related to disrupted interhemispheric communication in prefrontal, sensory, and parietal regions. This study provides evidence that structural alterations of several subregional callosal fibers in adults with TBI are associated with differential behavioral manifestations of bimanual motor functioning.

Diffusion tensor imaging metrics of the corpus callosum in relation to bimanual coordination: Effect of task complexity and sensory feedback

When manipulating objects with both hands, the corpus callosum (CC) is of paramount importance for interhemispheric information exchange. Hence, CC damage results in impaired bimanual performance. Here, healthy young adults performed a complex bimanual dial rotation task with or without augmented visual feedback and according to five interhand frequency ratios (1:1, 1:3, 2:3, 3:1, 3:2). The relation between bimanual task performance and microstructural properties of seven CC subregions (i.e., prefrontal, premotor/supplementary motor, primary motor, primary sensory, occipital, parietal, and temporal) was studied by means of diffusion tensor imaging (DTI). Findings revealed that bimanual coordination deteriorated in the absence as compared to the presence of augmented visual feedback. Simple frequency ratios (1:1) were performed better than the multifrequency ratios (non 1:1). Moreover, performance was more accurate when the preferred hand (1:3–2:3) as compared to the nonpreferred hand (3:1–3:2) moved faster and during noninteger (2:3–3:2) as compared to integer frequency ratios (1:3–3:1). DTI findings demonstrated that bimanual task performance in the absence of augmented visual feedback was significantly related to the microstructural properties of the primary motor and occipital region of the CC, suggesting that white matter microstructure is associated with the ability to perform bimanual coordination patterns in young adults. Hum Brain Mapp, 2013.

Microstructural organization of corpus callosum projections to prefrontal cortex predicts bimanual motor learning

The corpus callosum (CC) is the largest white matter tract in the brain. It enables interhemispheric communication, particularly with respect to bimanual coordination. Here, we use diffusion tensor imaging (DTI) in healthy humans to determine the extent to which structural organization of subregions within the CC would predict how well subjects learn a novel bimanual task. A single DTI scan was taken prior to training. Participants then practiced a bimanual visuomotor task over the course of 2 wk, consisting of multiple coordination patterns. Findings revealed that the predictive power of fractional anisotropy (FA) was a function of CC subregion and practice. That is, FA of the anterior CC, which projects to the prefrontal cortex, predicted bimanual learning rather than the middle CC regions, which connect primary motor cortex. This correlation was specific in that FA correlated significantly with performance of the most difficult frequency ratios tested and not the innately preferred, isochronous frequency ratio. Moreover, the effect was only evident after training and not at initiation of practice. This is the first DTI study in healthy adults which demonstrates that white matter organization of the interhemispheric connections between the prefrontal structures is strongly correlated with motor learning capability.

Correlations Between White Matter Integrity and Motor Function in Traumatic Brain Injury Patients

Background. Deterioration of motor function is one of several clinical manifestations following traumatic brain injury (TBI) in children and adolescents. Objective. To investigate the relationship between white matter (WM) integrity using diffusion tensor imaging (DTI) and motor functioning in young TBI patients. Methods. A group with moderate to severe TBI (n = 24) and a control group (n = 17) were scanned using DTI along with standard anatomical scans. Using ExploreDTI software, WM regions/tracts that carry efferent output (motor) from the brain were evaluated, as well as the corpus callosum, brainstem, internal capsule, and subcortical WM structures. Motor function was assessed using the Movement Assessment Battery for Children (M-ABC), consisting of manual dexterity, ball skills, and static and dynamic balance items. Results. TBI patients were less successful on the M-ABC than the controls and showed lower WM fractional anisotropy (FA) in the corpus callosum, anterior corona radiata, corticospinal tract, and cerebellum. Decreased FA was associated with lower motor performance in the TBI group but not in the control group. Conclusion. This study provides evidence for a structural alteration of motor pathways and regions in children and adolescents with TBI that are correlated with motor functioning. Further studies may be able to identify therapeutic targets and monitor the effects of new interventions.

Testing Multiple Coordination Constraints with a Novel Bimanual Visuomotor Task

The acquisition of a new bimanual skill depends on several motor coordination constraints. To date, coordination constraints have often been tested relatively independently of one another, particularly with respect to isofrequency and multifrequency rhythms. Here, we used a new paradigm to test the interaction of multiple coordination constraints. Coordination constraints that were tested included temporal complexity, directionality, muscle grouping, and hand dominance. Twenty-two healthy young adults performed a bimanual dial rotation task that required left and right hand coordination to track a moving target on a computer monitor. Two groups were compared, either with or without four days of practice with augmented visual feedback. Four directional patterns were tested such that both hands moved either rightward (clockwise), leftward (counterclockwise), inward or outward relative to each other. Seven frequency ratios (3∶1, 2∶1, 3∶2, 1∶1, 2∶3. 1∶2, 1∶3) between the left and right hand were introduced. As expected, isofrequency patterns (1∶1) were performed more successfully than multifrequency patterns (non 1∶1). In addition, performance was more accurate when participants were required to move faster with the dominant right hand (1∶3, 1∶2 and 2∶3) than with the non-dominant left hand (3∶1, 2∶1, 3∶2). Interestingly, performance deteriorated as the relative angular velocity between the two hands increased, regardless of whether the required frequency ratio was an integer or non-integer. This contrasted with previous finger tapping research where the integer ratios generally led to less error than the non-integer ratios. We suggest that this is due to the different movement topologies that are required of each paradigm. Overall, we found that this visuomotor task was useful for testing the interaction of multiple coordination constraints as well as the release from these constraints with practice in the presence of augmented visual feedback.

Disturbed cortico-subcortical interactions during motor task switching in traumatic brain injury.

The ability to suppress and flexibly adapt motor behavior is a fundamental mechanism of cognitive control, which is impaired in traumatic brain injury (TBI). Here, we used a combination of functional magnetic resonance imaging and diffusion weighted imaging tractography to study changes in brain function and structure associated with motor switching performance in TBI. Twenty‐three young adults with moderate‐severe TBI and twenty‐six healthy controls made spatially and temporally coupled bimanual circular movements. A visual cue signaled the right hand to switch or continue its circling direction. The time to initiate the switch (switch response time) was longer and more variable in the TBI group and TBI patients exhibited a higher incidence of complete contralateral (left hand) movement disruptions. Both groups activated the basal ganglia and a previously described network for task‐set implementation, including the supplementary motor complex and bilateral inferior frontal cortex (IFC). Relative to controls, patients had significantly increased activation in the presupplementary motor area (preSMA) and left IFC, and showed underactivation of the subthalamic nucleus (STN) region. This altered functional engagement was related to the white matter microstructural properties of the tracts connecting preSMA, IFC, and STN. Both functional activity in preSMA, IFC, and STN, and the integrity of the connections between them were associated with behavioral performance across patients and controls. We suggest that damage to these key pathways within the motor switching network because of TBI, shifts the patients toward the lower end of the existing structure‐function‐behavior spectrum. Hum Brain Mapp, 2013.