Dataset Information

Disuse-driven plasticity in the human thalamus and putamen.

ABSTRACT: Cortico-striato-thalamo-cortical loops have been heavily studied because of their importance in movement disorders such as Parkinson's Disease and tremor. Capturing plasticity effect in this circuit has been mainly successful using animals or using invasive electrophysiology in patients. Given the importance of the striatum and thalamus for motor control and skill learning, the current study leverages on an arm immobilization paradigm in humans with neuroimaging to induce disuse and explore human subcortical motor circuits plasticity. We employed an experimental paradigm involving upper-extremity immobilization for two weeks with daily resting-state functional connectivity (FC) and motor task-related fMRI. This approach of dense sampling of individuals, i.e Precision Functional Mapping (PFM), offers individual-specific insights and provides enough data to address the issue of low signal to noise ratio in the subcortex. Previously, we identified increased FC between somatomotor cortex and the cingulo-opercular network and emergence of disuse pulses in the cortex during casting. We expand our prior investigation to include analysis adapted to the signal characteristic of subcortical regions to capture disuse-driven plasticity in human subcortical circuits. Subcortical nodes, particularly the central thalamus and posterior putamen, exhibited strengthened FC during disuse and spontaneous activity pulses. Motor task fMRI validated that subcortical disuse-driven plasticity effects spatially correspond to the upper extremity movement execution circuitry, emphasizing the role of these structures in motor control and adaptation. In conclusion, our study highlights the involvement of the cortico-striato-thalamo-cortical loops in human motor plasticity and discuss similarities in findings with two research fields: Parkinson Disease (PD), suggesting a novel interpretation of PD neuroimaging finding; and sleep, particularly plasticity and sleep pressure regulated by the thalamus.

SUBMITTER: Chauvin RJ

PROVIDER: S-EPMC10659348 | biostudies-literature | 2023 Nov

REPOSITORIES: biostudies-literature

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Disuse-driven plasticity in the human thalamus and putamen.

Chauvin Roselyne J RJ Newbold Dillan J DJ Nielsen Ashley N AN Miller Ryland L RL Krimmel Samuel R SR Metoki Athanasia A Wang Anxu A Van Andrew N AN Montez David F DF Marek Scott S Suljic Vahdeta V Baden Noah J NJ Ramirez-Perez Nadeshka N Scheidter Kristen M KM Monk Julia S JS Whiting Forrest I FI Adeyemo Babatunde B Snyder Abraham Z AZ Kay Benjamin P BP Raichle Marcus E ME Laumann Timothy O TO Gordon Evan M EM Dosenbach Nico U F NUF

bioRxiv : the preprint server for biology 20240125

Motor adaptation in cortico-striato-thalamo-cortical loops has been studied mainly in animals using invasive electrophysiology. Here, we leverage functional neuroimaging in humans to study motor circuit plasticity in the human subcortex. We employed an experimental paradigm that combined two weeks of upper-extremity immobilization with daily resting-state and motor task fMRI before, during, and after the casting period. We previously showed that limb disuse leads to decreased functional connecti ...[more]

PMID: 37987000

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Project description:BackgroundThe thalamus and the putamen are highly connected hubs implicated in multiple sclerosis (MS) pathology. It remains unclear if white matter (WM) tracts, which pass through them, have a different susceptibility to MS pathology, and if so, if their impact on disability predominates over that exerted by disease in other WM tracts. We hypothesized that WM tracts connected to and passing through these hubs (subsequently termed hub+ tracts) would be more susceptible to MS-related pathology than tracts that do not pass through them (hub- tracts) due to retrograde and anterograde distant degeneration. Thus, we compared the lesion load and neurite orientation dispersion and density imaging (NODDI) derived metrics between hub+ and hub- tracts and assessed the relationship between these MRI metrics and those of physical impairment.MethodsEighteen patients (mean age of 45.5 years, 12 females) had 3 Tesla MRI consisting of T1-weighted and T2-weighted Fluid Attenuated Inversion Recovery (FLAIR), and NODDI from which the orientation dispersion index (ODI), neurite density index (NDI), and isotropic volume fraction (IVF) were derived. Forty-nine WM tracts, i.e., 12 hub+ and 37 hub- tracts, were segmented out. Exploratory analyses of the differences in lesion burden, whole tract and normal appearing WM (NAWM) NODDI metrics were carried out between the two types of tracts using a Mann-Whitney U test. Correlations with physical impairment, quantified using the expanded disability status scale (EDSS) and timed 25-foot walk (T25FW) test were assessed using Spearman correlation analyses.ResultsHub- tracts had larger T1- (p<0.001) and T2-lesion (p<0.001) volumes; lower ODI (p<0.001), NDI (p<0.001) and higher IVF (p = 0.020) in comparison to hub+ tracts. Measures of tissue injury in hub+ tracts correlated with those of clinical disability, though less strongly than in hub- tracts.ConclusionsContrary to our hypothesis, our exploratory pilot study results suggest that WM tracts that overlap with the thalamus and the putamen have a lower degree of lesional and non-lesional tissue injury, suggesting a protective role of the hubs against MS pathology or a higher degree of vulnerability of those not passing through hub stations. We also show a weaker association between disability impairment and hub+ pathology, compared to that in hub- tracts. Our findings point to a potential role of disease location in relation to hubs as guidance for treatment personalization in MS.

Project description:Previous MRI studies confirmed abnormalities in the limbic-cortical-striatal-pallidal-thalamic (LCSPT) network or limbic-cortico-striatal-thalamic-cortical (LCSTC) circuits in patients with major depressive disorder (MDD), but few studies have investigated the subcortical structural abnormalities. Therefore, we sought to determine whether focal subcortical grey matter (GM) changes might be present in MDD at an early stage. We recruited 30 first episode, untreated patients with major depressive disorder (MDD) and 26 healthy control subjects. Voxel-based morphometry was used to evaluate cortical grey matter changes, and automated volumetric and shape analyses were used to assess volume and shape changes of the subcortical GM structures, respectively. In addition, probabilistic tractography methods were used to demonstrate the relationship between the subcortical and the cortical GM. Compared to healthy controls, MDD patients had significant volume reductions in the bilateral putamen and left thalamus (FWE-corrected, p < 0.05). Meanwhile, the vertex-based shape analysis showed regionally contracted areas on the dorsolateral and ventromedial aspects of the bilateral putamen, and on the dorsal and ventral aspects of left thalamus in MDD patients (FWE-corrected, p < 0.05). Additionally, a negative correlation was found between local atrophy in the dorsal aspects of the left thalamus and clinical variables representing severity. Furthermore, probabilistic tractography demonstrated that the area of shape deformation of the bilateral putamen and left thalamus have connections with the frontal and temporal lobes, which were found to be related to major depression. Our results suggested that structural abnormalities in the putamen and thalamus might be present in the early stages of MDD, which support the role of subcortical structure in the pathophysiology of MDD. Meanwhile, the present study showed that these subcortical structural abnormalities might be the potential trait markers of MDD.

Project description:ObjectiveCortical atrophy close to medial temporal structures has been described consistently in patients with temporal lobe epilepsy (TLE). Successful TLE surgery may have a neuroprotective effect preventing further atrophy of temporal and extratemporal cortex. However, the effects of epilepsy surgery on subcortical structures demand additional enlightenment. This work aimed to determine how epilepsy surgery affects volumes of subcortical structures in medically refractory temporal lobe epilepsy patients.MethodsWe compared MRI volumes of subcortical structures in 62 patients with TLE (36 left, 26 right) before and after anterior temporal lobectomy with 38 TLE patients (20 left, 18 right) who were considered to be good surgical candidates and had at least two brain MRIs.ResultsThere were no volume differences in subcortical structures on preoperative and initial MRIs of non-operated TLE patients. At baseline, the ipsilateral thalamus and putamen in TLE patients were marginally smaller than contralateral structures. Operated patients showed a significant postoperative volume reduction in ipsilateral thalamus, putamen, and globus pallidus. In contrast, there were no significant volumetric reductions in non-operated patients longitudinally. There were no volumetric changes associated with different surgical outcomes or different postoperative cognitive outcomes.SignificanceOur study demonstrated postoperative volume loss of thalamus, putamen and globus pallidus ipsilaterally to the side of resection. Our findings suggest surgery-related changes, likely Wallerian degeneration within subcortical networks not related to seizure or cognitive outcome.Plain language summaryWe studied 100 patients with epilepsy, comparing those who had surgery to those who did not. After surgery, the thalamus, putamen and globus pallidus on the same side as the surgery shrank significantly, but not in non-surgery patients. This suggests surgery-related changes in deeper brain structures, unrelated to seizure freedom or cognitive outcomes. This research sheds additional light on the response of the subcortical structure to epilepsy surgery, highlighting potential areas for further study.

Dataset Information

Disuse-driven plasticity in the human thalamus and putamen.

Publications

Disuse-driven plasticity in the human thalamus and putamen.

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