Changes in regional activity are accompanied with changes in inter-regional connectivity during 4 weeks motor learning

Ma, Liangsuo; Wang, Binquan; Narayana, Shalini; Hazeltine, Eliot; Chen, Xiying; Robin, Donald A.; Fox, Peter T.; Xiong, Jinhu

doi:10.1016/j.brainres.2009.12.073

Cited by 135 publications

(110 citation statements)

References 106 publications

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“…basal ganglia increased with practice (Ma et al, 2010). However, with the present design, we cannot single out any particular component of the activated network as being responsible for the potential clinical benefits.…”

Section: Discussionmentioning

confidence: 98%

Real-Time Functional Magnetic Resonance Imaging Neurofeedback for Treatment of Parkinson's Disease

Subramanian¹,

Hindle²,

Johnston³

et al. 2011

J. Neurosci.

237

221

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Self-regulation of brain activity in humans based on real-time feedback of functional magnetic resonance imaging (fMRI) signal is emerging as a potentially powerful, new technique. Here, we assessed whether patients with Parkinson's disease (PD) are able to alter local brain activity to improve motor function. Five patients learned to increase activity in the supplementary motor complex over two fMRI sessions using motor imagery. They attained as much activation in this target brain region as during a localizer procedure with overt movements. Concomitantly, they showed an improvement in motor speed (finger tapping) and clinical ratings of motor symptoms (37% improvement of the motor scale of the Unified Parkinson's Disease Rating Scale). Activation during neurofeedback was also observed in other cortical motor areas and the basal ganglia, including the subthalamic nucleus and globus pallidus, which are connected to the supplementary motor area (SMA) and crucial nodes in the pathophysiology of PD. A PD control group of five patients, matched for clinical severity and medication, underwent the same procedure but did not receive feedback about their SMA activity. This group attained no control of SMA activation and showed no motor improvement. These findings demonstrate that self-modulation of corticosubcortical motor circuits can be achieved by PD patients through neurofeedback and may result in clinical benefits that are not attainable by motor imagery alone.

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Section: Discussionmentioning

confidence: 98%

Real-Time Functional Magnetic Resonance Imaging Neurofeedback for Treatment of Parkinson's Disease

Subramanian¹,

Hindle²,

Johnston³

et al. 2011

J. Neurosci.

237

221

View full text Add to dashboard Cite

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“…For example, Stevens et al (69) reported stronger coupling between the inferior frontal gyrus and face-preferential areas of the visual cortex after a face-recognition task, as well as stronger coupling between the inferior frontal gyrus and scene-specific visual areas after a scene-recognition task. Ma et al (70), using independent component analysis after extended motor-sequence learning, showed increased strength in three motor-related components, which tracked behavioral improvement. A recent study by Mackey et al (71) reported strengthened correlations between frontal and parietal attention and control regions in subjects who completed a lengthy preparation course for a law-school entrance examination.…”

Section: Discussionmentioning

confidence: 99%

Brain aerobic glycolysis and motor adaptation learning

Shannon

Vaishnavi

Vlassenko

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

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Ten percent to 15% of glucose used by the brain is metabolized nonoxidatively despite adequate tissue oxygenation, a process termed aerobic glycolysis (AG). Because of the known role of glycolysis in biosynthesis, we tested whether learning-induced synaptic plasticity would lead to regionally appropriate, learningdependent changes in AG. Functional MRI (fMRI) before, during, and after performance of a visual-motor adaptation task demonstrated that left Brodmann area 44 (BA44) played a key role in adaptation, with learning-related changes to activity during the task and altered resting-state, functional connectivity after the task. PET scans before and after task performance indicated a sustained increase in AG in left BA 44 accompanied by decreased oxygen consumption. Intersubject variability in behavioral adaptation rate correlated strongly with changes in AG in this region, as well as functional connectivity, which is consistent with a role for AG in synaptic plasticity.T he resting brain's energy needs are supported almost entirely by the metabolism of glucose to carbon dioxide and water (1). The first step of this process, glycolysis, requires no oxygen whereas the second step, oxidative phosphorylation, does. In the normal adult human brain, 10-15% of the glucose never reaches the second step-it is shunted away from oxidative phosphorylation despite the presence of adequate oxygen (2-5). This process is commonly referred to as aerobic glycolysis (AG).Several roles for AG have been identified, including biosynthesis (for recent reviews, see refs. 6-8), the regulation of cellular redox states (9, 10), the regulation of apoptosis (11), the provision of ATP for membrane pumps (12)(13)(14), and the regulation of cell excitability (15, 16). More recently, similar functions of AG have been observed in the posttranscriptional control of T-cell effector function (17, 18), an observation now extended to the microglia (19), where it is associated with an activated state related to inflammation as well as synaptic pruning.In the developing human brain, at a time when synaptic growth rates are highest (approximately age 10), total glucose consumption is twice that of the adult, and 30% of that glucose consumption is AG (a recent summary of this early literature is contained in ref. 20), suggesting an important role in brain development. Another remarkable feature of AG in the adult human brain is that it varies regionally (21): nearly 25% of resting glucose consumption in the medial prefrontal cortex is AG whereas AG constitutes as little as 2% glucose consumption in the cerebellum and medial temporal lobes. Correlation of these regional data with regional gene expression in the adult human brain revealed increased gene expression typical of infancy (i.e., neotony) that is related to synapse formation and growth (20).Further supporting the link between AG and plasticity are findings demonstrating that lactate, released by astrocytes and taken up by neurons, is critical for memory formation. Neuronal uptake of lactate ch...

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“…Previous studies have demonstrated that inter-regional brain connectivity can change rapidly after just one session of motor practice (Wu et al, 2008), and then evolve gradually over the next few days (Song et al, 2011), and may last for several weeks (Ma et al, 2010). Functional connectivity has been shown to predict how well an individual learns cognitive or motor tasks (Henson et al, 1999;Wu et al, 2008) and may index functional decline as a result of aging (Cook et al, 2007).…”

Section: Discussionmentioning

confidence: 99%

“…We examined functional connectivity with respect to DLPFC and PMd in older and younger adults during the retrieval of motor sequences learned under interleaved compared with those learned under RP. Given that the strength of brain functional connectivity is a function of learning (Ma et al, 2010), we hypothesized that practice under CI conditions may increase prefrontal and premotor connectivity with other brain regions, which in turn, enhances retrieval of sequences. Through the PPI analysis, we found that older and younger adults relied on different patterns of functional connectivity for this benefit.…”

mentioning

confidence: 99%

Enhanced Motor Learning in Older Adults Is Accompanied by Increased Bilateral Frontal and Fronto-Parietal Connectivity

Lin

Chiang

et al. 2012

Brain Connectivity

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We recently demonstrated that older adults can benefit as much as younger adults from learning skills in an interleaved manner. Here we investigate whether optimized learning through interleaved practice (IP) is associated with changes in inter-regional brain connectivity and whether younger and older adults differ in such brainbehavior correlations. Younger and older adults practiced a set of three 4-element motor sequences in a repetitive or in an interleaved order for 2 consecutive days. Retention of the practiced sequences was evaluated 3 days after practice with functional images acquired simultaneously. A within-subject design was used so that subjects practiced sequences in the other condition (repetitive or interleaved) 2-4 weeks later. Using the psychophysiological interaction (PPI) analysis approach, we found that IP led to higher functional connectivity between the right and left dorsal lateral prefrontal cortex (DLPFC) and between the dorsal premotor cortex (PMd) and inferior parietal lobule (IPL) in older adults. Moreover, increased connectivity between these regions was significantly associated with the learning benefits of IP. In contrast, in younger adults, enhanced learning as a result of IP was associated with increased connectivity between DLPFC and the supplementary motor area (SMA) and the inferior frontal gyrus. These data suggest that though younger and older gain similar behavioral benefits from interleaved training, aging may alter the operation of brain networks underlying such optimized learning.

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Changes in regional activity are accompanied with changes in inter-regional connectivity during 4 weeks motor learning

Cited by 135 publications

References 106 publications

Real-Time Functional Magnetic Resonance Imaging Neurofeedback for Treatment of Parkinson's Disease

Real-Time Functional Magnetic Resonance Imaging Neurofeedback for Treatment of Parkinson's Disease

Brain aerobic glycolysis and motor adaptation learning

Enhanced Motor Learning in Older Adults Is Accompanied by Increased Bilateral Frontal and Fronto-Parietal Connectivity

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