Michael W. Parsons

Distinct neural systems underlie learning visuomotor and spatial representations of motor skills

Motor skill learning depends upon acquiring knowledge about multiple features of sequential behaviors, including their visuomotor and spatial properties. To investigate the neural systems that distinguish these representations, we carried out functional magnetic resonance imaging (fMRI) as healthy adults learned to type sequences on a novel keyboard. On the initial training day, learning‐related changes in brain activation were found in distributed cortical regions, only a subset of which correlated with improvements in movement time (MT), suggesting their preeminence in controlling movements online. Subjects received extended training on the sequences during the ensuing week, after which they returned to the scanner for another imaging session. Relative to performance at the end of the first training day, continued plasticity was most striking in the inferior parietal cortex and new areas of plasticity were uncovered in the caudate and cerebellum. Plasticity in these regions correlated with reaction time (RT), suggesting their role in planning sequences before movement onset. Two transfer conditions probed for “what” subjects learned. The probe for visuomotor learning produced increased activation in visual analysis (left inferior visual cortex) and advance planning (left caudate) systems. The probe for spatial learning produced increased activation in visuomotor‐transformation (left dorsal visual pathway) and retrieval (left precuneus) systems. Increased activity in all of these regions correlated with increased RT, but not MT, indicating that both transfer conditions interfered with the neural representation of plans for the sequences, but not processes that controlled their implementation. These findings demonstrated that neuroanatomically dissociable systems support the acquisition of visuomotor and spatial representations of actions. Hum Brain Mapping 24:229–247, 2005.

Neural activation during response inhibition differentiates blast from mechanical causes of mild to moderate traumatic brain injury.

Military personnel involved in Operations Enduring Freedom and Iraqi Freedom (OEF/OIF) commonly experience blast-induced mild to moderate traumatic brain injury (TBI). In this study, we used task-activated functional MRI (fMRI) to determine if blast-related TBI has a differential impact on brain activation in comparison with TBI caused primarily by mechanical forces in civilian settings. Four groups participated: (1) blast-related military TBI (milTBI; n=21); (2) military controls (milCON; n=22); (3) non-blast civilian TBI (civTBI; n=21); and (4) civilian controls (civCON; n=23) with orthopedic injuries. Mild to moderate TBI (MTBI) occurred 1 to 6 years before enrollment. Participants completed the Stop Signal Task (SST), a measure of inhibitory control, while undergoing fMRI. Brain activation was evaluated with 2 (mil, civ)×2 (TBI, CON) analyses of variance, corrected for multiple comparisons. During correct inhibitions, fMRI activation was lower in the TBI than CON subjects in regions commonly associated with inhibitory control and the default mode network. In contrast, inhibitory failures showed significant interaction effects in the bilateral inferior temporal, left superior temporal, caudate, and cerebellar regions. Specifically, the milTBI group demonstrated more activation than the milCON group when failing to inhibit; in contrast, the civTBI group exhibited less activation than the civCON group. Covariance analyses controlling for the effects of education and self-reported psychological symptoms did not alter the brain activation findings. These results indicate that the chronic effects of TBI are associated with abnormal brain activation during successful response inhibition. During failed inhibition, the pattern of activation distinguished military from civilian TBI, suggesting that blast-related TBI has a unique effect on brain function that can be distinguished from TBI resulting from mechanical forces associated with sports or motor vehicle accidents. The implications of these findings for diagnosis and treatment of TBI are discussed.

Corpus Callosum Volume in Railroad Workers With Chronic Exposure to Solvents

Objective: Changes to cognition and behavior have been reported after long-term exposure to solvents. Solvents are hypothesized to affect brain white matter. To test this, we examined the volume of the corpus callosum in workers with a history of exposure to solvents. Methods: We manually traced (blind to group membership) the volume of the corpus callosum in 31 railroad workers and 31 matched controls. Results: There was a decrease in the genu of the corpus callosum in the solvent-exposed workers compared with controls. A smaller volume of the genu of the corpus callosum was associated with greater exposure and worse performance on cognitive tasks. Conclusions: This study supports the hypothesis that occupational exposure to solvents affects the anterior white matter of the brain and is related to extent of exposure and degree of cognitive change.

Anterior Medial Temporal Lobe Activation during Encoding of Words: FMRI Methods to Optimize Sensitivity.

The existence of a rostrocaudal gradient of medial temporal lobe (MTL) activation during memory encoding has historically received support from positron emission tomography studies, but less so from functional MRI (FMRI) studies. More recently, FMRI studies have demonstrated that characteristics of the stimuli can affect the location of activation seen in the MTL when those stimuli are encoded. The current study tested the hypothesis that MTL activation during memory encoding is related to the modality of stimulus presentation. Subjects encoded auditorily or visually presented words in an FMRI novelty paradigm. Imaging and analysis parameters were optimized to minimize susceptibility artifact in the anterior MTL. Greater activation was observed in the anterior than posterior MTL for both modalities of stimulus presentation. The results indicate that anterior MTL activation occurred during encoding, independent of stimulus modality and provide support for the hypothesis that verbal-semantic memory processing occurs in anterior MTL. The authors suggest that technical factors are critical for observing the rostrocaudal gradient in MTL memory activation.

Motor demand-dependent activation of ipsilateral motor cortex

The role of ipsilateral primary motor cortex (M1) in hand motor control during complex task performance remains controversial. Bilateral M1 activation is inconsistently observed in functional (f)MRI studies of unilateral hand performance. Two factors limit the interpretation of these data. As the motor tasks differ qualitatively in these studies, it is conceivable that M1 contributions differ with the demand on skillfulness. Second, most studies lack the verification of a strictly unilateral execution of the motor task during the acquisition of imaging data. Here, we use fMRI to determine whether ipsilateral M1 activity depends on the demand for precision in a pointing task where precision varied quantitatively while movement trajectories remained equal. Thirteen healthy participants used an MRI-compatible joystick to point to targets of four different sizes in a block design. A clustered acquisition technique allowed simultaneous fMRI/EMG data collection and confirmed that movements were strictly unilateral. Accuracy of performance increased with target size. Overall, the pointing task revealed activation in contralateral and ipsilateral M1, extending into contralateral somatosensory and parietal areas. Target size-dependent activation differences were found in ipsilateral M1 extending into the temporal/parietal junction, where activation increased with increasing demand on accuracy. The results suggest that ipsilateral M1 is active during the execution of a unilateral motor task and that its activity is modulated by the demand on precision.

Disruption of caudate working memory activation in chronic blast-related traumatic brain injury

Mild to moderate traumatic brain injury (TBI) due to blast exposure is frequently diagnosed in veterans returning from the wars in Iraq and Afghanistan. However, it is unclear whether neural damage resulting from blast TBI differs from that found in TBI due to blunt-force trauma (e.g., falls and motor vehicle crashes). Little is also known about the effects of blast TBI on neural networks, particularly over the long term. Because impairment in working memory has been linked to blunt-force TBI, the present functional magnetic resonance imaging (fMRI) study sought to investigate whether brain activation in response to a working memory task would discriminate blunt-force from blast TBI. Twenty-five veterans (mean age = 29.8 years, standard deviation = 6.01 years, 1 female) who incurred TBI due to blast an average of 4.2 years prior to enrollment and 25 civilians (mean age = 27.4 years, standard deviation = 6.68 years, 4 females) with TBI due to blunt-force trauma performed the Sternberg Item Recognition Task while undergoing fMRI. The task involved encoding 1, 3, or 5 items in working memory. A group of 25 veterans (mean age = 29.9 years, standard deviation = 5.53 years, 0 females) and a group of 25 civilians (mean age = 27.3 years, standard deviation = 5.81 years, 0 females) without history of TBI underwent identical imaging procedures and served as controls. Results indicated that the civilian TBI group and both control groups demonstrated a monotonic relationship between working memory set size and activation in the right caudate during encoding, whereas the blast TBI group did not (p < 0.05, corrected for multiple comparisons using False Discovery Rate). Blast TBI was also associated with worse performance on the Sternberg Item Recognition Task relative to the other groups, although no other group differences were found on neuropsychological measures of episodic memory, inhibition, and general processing speed. These results could not be attributed to caudate atrophy or the presence of PTSD symptoms. Our results point to a specific vulnerability of the caudate to blast injury. Changes in activation during the Sternberg Item Recognition Task, and potentially other tasks that recruit the caudate, may serve as biomarkers for blast TBI.

Whole-hand sensorimotor area: cortical stimulation localization and correlation with functional magnetic resonance imaging

OBJECT The pli de passage moyen (PPM) is an omega-shaped cortical landmark bulging into the central sulcus. There has been considerable interest in the PPM given that hand motor and sensory tasks have been found on functional magnetic resonance (fMR) imaging to activate the structure. Note, however, that the cortical function subserved by the PPM is not completely understood. Finger and thumb function are somatotopically organized over the central area and encompass a larger cortical surface than the anatomical PPM. Therefore, a sensory or motor hand area within the PPM would be redundant with the somatotopically organized digit function in the primary sensorimotor cortex. In this study the authors aimed to clarify the function subserved by the PPM and further evaluate hand area function in the primary sensorimotor cortex. METHODS To further elucidate the function subserved by the PPM, patients underwent cortical stimulation in the region of the PPM as well as fMR imaging-demonstrated activation of the hand area. Two separate analytical methods were used to correlate hand area functional imaging with whole-hand sensory and motor responses induced by cortical stimulation. RESULTS A relationship of the anatomical PPM with cortical stimulation responses as well as hand fMR imaging activation was observed. CONCLUSIONS A strong relationship was identified between the PPM, whole-hand sensory and motor stimulation responses, and fMR imaging hand activation. Whole-hand motor and whole-hand sensory cortical regions were identified in the primary sensorimotor cortex. It was localized to the PPM and exists in addition to the somatotopically organized finger and thumb sensory and motor areas.

White Matter Correlates of Cognitive Capacity Studied With Diffusion Tensor Imaging: Implications for Cognitive Reserve

Cognitive reserve (CR) is a theoretical concept used to explain and study individual differences in cognitive symptom expression in neurological disease. In the absence of neurologic injury or demands on processing, compensatory and protective factors may be considered to represent cognitive capacity (CC), rather than cognitive reserve, per se. We studied the white matter structural correlates of CC in 51 young, healthy participants. White matter structural correlates were obtained from fractional anisotropy (FA) measures using diffusion tensor imaging (DTI). CC was represented by intelligence, reading ability, and years of education, commonly used measures for studying CR. CC was positively correlated with FA in the right posterior inferior longitudinal fasciculus. We observed gender differences in FA (males > females) and tested for gender differences in FA correlates of CC. However, the interaction between gender and CC for areas of FA was not significant. Our data indicate that in the healthy young brain, greater CC correlates with higher FA values in a focal area that does not significantly differ by gender.

The role of the mammillary bodies in memory : A case of amnesia following bilateral resection

Background and Objectives: Craniopharyngioma (CP) patients typically show good neuropsychiatric outcome following tumor resection. We present the case of a 51-year old woman who sustained damage to white matter pathways during surgery resulting in a disconnection of the Papez circuit (loss of bilateral mammillary bodies, columns of the fomix and mammillothalamic tracts). Methods and Results: Neuropsychological evaluations were completed at 10 and 30 weeks post-operatively, and indicated both retrograde and severe anterograde amnesia, as well as persistent depression. At the second evaluation, most cognitive deficits had improved, but memory and mood deficits remained. Metamemory and priming remained intact. Conclusions: This case illustrates a profound neuropsychiatric morbidity associated with a surgery that is typically considered benign and confirms the well-known dissociation between explicit recollection of newly learned information and less conscious forms of learning and memory. This rare pathology provides further information regarding the role of the mammillary bodies in memory.

Neural activation during frequency-memory performance.

Lesion studies have demonstrated that frequency memory, or memory for the frequency of occurrence, is associated with prefrontal and not temporal lobe lesions. This study examined neural activation during performance on a frequency-memory-judgment task and a recognition-memory task, both using words. Relative to a control task, the authors observed peaks of activation during frequency-memory performance in the left ventrolateral prefrontal cortex (BA 45) and other areas typically associated with working memory (dorsolateral prefrontal cortex, posterior parietal cortex). Recognition performance was associated with activation in the same left ventrolateral prefrontal location as was observed with frequency memory. When comparing activation during frequency memory with activation during recognition memory, the authors found a suppression of activation in the hippocampus bilaterally during frequency memory. This study supports a neuroanatomical distinction between frequency and recognition memory.