Dataset Information

A Direct Cortico-Nigral Pathway as Revealed by Constrained Spherical Deconvolution Tractography in Humans.

ABSTRACT: Substantia nigra is an important neuronal structure, located in the ventral midbrain, that exerts a regulatory function within the basal ganglia circuitry through the nigro-striatal pathway. Although its subcortical connections are relatively well-known in human brain, little is known about its cortical connections. The existence of a direct cortico-nigral pathway has been demonstrated in rodents and primates but only hypothesized in humans. In this study, we aimed at evaluating cortical connections of substantia nigra in vivo in human brain by using probabilistic constrained spherical deconvolution (CSD) tractography on magnetic resonance diffusion weighted imaging data. We found that substantia nigra is connected with cerebral cortex as a whole, with the most representative connections involving prefrontal cortex, precentral and postcentral gyri and superior parietal lobule. These results may be relevant for the comprehension of the pathophysiology of several neurological disorders involving substantia nigra, such as parkinson's disease, schizophrenia, and pathological addictions.

SUBMITTER: Cacciola A

PROVIDER: S-EPMC4960230 | biostudies-literature | 2016

REPOSITORIES: biostudies-literature

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A Direct Cortico-Nigral Pathway as Revealed by Constrained Spherical Deconvolution Tractography in Humans.

Cacciola Alberto A Milardi Demetrio D Anastasi Giuseppe P GP Basile Gianpaolo A GA Ciolli Pietro P Irrera Mariangela M Cutroneo Giuseppina G Bruschetta Daniele D Rizzo Giuseppina G Mondello Stefania S Bramanti Placido P Quartarone Angelo A

Frontiers in human neuroscience 20160726

Substantia nigra is an important neuronal structure, located in the ventral midbrain, that exerts a regulatory function within the basal ganglia circuitry through the nigro-striatal pathway. Although its subcortical connections are relatively well-known in human brain, little is known about its cortical connections. The existence of a direct cortico-nigral pathway has been demonstrated in rodents and primates but only hypothesized in humans. In this study, we aimed at evaluating cortical connect ...[more]

PMID: 27507940

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Project description:Parkinson's disease (PD) is a progressive neurodegenerative disorder that affects extensive regions of the central nervous system. In this work, we evaluated the structural connectome of patients with PD, as mapped by diffusion-weighted MRI tractography and a multi-shell, multi-tissue (MSMT) constrained spherical deconvolution (CSD) method to increase the precision of tractography at tissue interfaces. The connectome was mapped with probabilistic MSMT-CSD in 21 patients with PD and in 21 age- and gender-matched controls. Mapping was also performed by deterministic single-shell, single tissue (SSST)-CSD tracking and probabilistic SSST-CSD tracking for comparison. A support vector machine was trained to predict diagnosis based on a linear combination of graph metrics. We showed that probabilistic MSMT-CSD could detect significantly reduced global strength, efficiency, clustering, and small-worldness, and increased global path length in patients with PD relative to healthy controls; by contrast, probabilistic SSST-CSD only detected the difference in global strength and small-worldness. In patients with PD, probabilistic MSMT-CSD also detected a significant reduction in local efficiency and detected clustering in the motor, frontal temporoparietal associative, limbic, basal ganglia, and thalamic areas. The network-based statistic identified a subnetwork of reduced connectivity by MSMT-CSD and probabilistic SSST-CSD in patients with PD, involving key components of the cortico-basal ganglia-thalamocortical network. Finally, probabilistic MSMT-CSD had superior diagnostic accuracy compared with conventional probabilistic SSST-CSD and deterministic SSST-CSD tracking. In conclusion, probabilistic MSMT-CSD detected a greater extent of connectome pathology in patients with PD, including those with cortico-basal ganglia-thalamocortical network disruptions. Connectome analysis based on probabilistic MSMT-CSD may be useful when evaluating the extent of white matter connectivity disruptions in PD.

Project description:Virtual dissection of white matter (WM) using diffusion MRI tractography is confounded by its poor reproducibility. Despite the increased adoption of advanced reconstruction models, early region-of-interest driven protocols based on diffusion tensor imaging (DTI) remain the dominant reference for virtual dissection protocols. Here we bridge this gap by providing a comprehensive description of typical WM anatomy reconstructed using a reproducible automated subject-specific parcellation-based approach based on probabilistic constrained-spherical deconvolution (CSD) tractography. We complement this with a WM template in MNI space comprising 68 bundles, including all associated anatomical tract selection labels and associated automated workflows. Additionally, we demonstrate bundle inter- and intra-subject variability using 40 (20 test-retest) datasets from the human connectome project (HCP) and 5 sessions with varying b-values and number of b-shells from the single-subject Multiple Acquisitions for Standardization of Structural Imaging Validation and Evaluation (MASSIVE) dataset. The most reliably reconstructed bundles were the whole pyramidal tracts, primary corticospinal tracts, whole superior longitudinal fasciculi, frontal, parietal and occipital segments of the corpus callosum and middle cerebellar peduncles. More variability was found in less dense bundles, e.g., the fornix, dentato-rubro-thalamic tract (DRTT), and premotor pyramidal tract. Using the DRTT as an example, we show that this variability can be reduced by using a higher number of seeding attempts. Overall inter-session similarity was high for HCP test-retest data (median weighted-dice = 0.963, stdev = 0.201 and IQR = 0.099). Compared to the HCP-template bundles there was a high level of agreement for the HCP test-retest data (median weighted-dice = 0.747, stdev = 0.220 and IQR = 0.277) and for the MASSIVE data (median weighted-dice = 0.767, stdev = 0.255 and IQR = 0.338). In summary, this WM atlas provides an overview of the capabilities and limitations of automated subject-specific probabilistic CSD tractography for mapping white matter fasciculi in healthy adults. It will be most useful in applications requiring a reproducible parcellation-based dissection protocol, and as an educational resource for applied neuroimaging and clinical professionals.

Project description:IntroductionCortico-cortical evoked potentials (CCEPs) are utilized to identify effective networks in the human brain. Following single-pulse electrical stimulation of cortical electrodes, evoked responses are recorded from distant cortical areas. A negative deflection (N1) which occurs 10-50 ms post-stimulus is considered to be a marker for direct cortico-cortical connectivity. However, with CCEPs alone it is not possible to observe the white matter pathways that conduct the signal or accurately predict N1 amplitude and latency at downstream recoding sites. Here, we develop a new approach, termed "dynamic tractography," which integrates CCEP data with diffusion-weighted imaging (DWI) data collected from the same patients. This innovative method allows greater insights into cortico-cortical networks than provided by each method alone and may improve the understanding of large-scale networks that support cognitive functions. The dynamic tractography model produces several fundamental hypotheses which we investigate: 1) DWI-based pathlength predicts N1 latency; 2) DWI-based pathlength negatively predicts N1 voltage; and 3) fractional anisotropy (FA) along the white matter path predicts N1 propagation velocity.MethodsTwenty-three neurosurgical patients with drug-resistant epilepsy underwent both extraoperative CCEP recordings and preoperative DWI scans. Subdural grids of 3 mm diameter electrodes were used for stimulation and recording, with 98-128 eligible electrodes per patient. CCEPs were elicited by trains of 1 Hz stimuli with an intensity of 5 mA and recorded at a sample rate of 1 kHz. N1 peak and latency were defined as the maximum of a negative deflection within 10-50 ms post-stimulus with a z-score > 5 relative to baseline. Electrodes and DWI were coregistered to construct electrode connectomes for white matter quantification.ResultsClinical variables (age, sex, number of anti-epileptic drugs, handedness, and stimulated hemisphere) did not correlate with the key outcome measures (N1 peak amplitude, latency, velocity, or DWI pathlength). All subjects and electrodes were therefore pooled into a group-level analysis to determine overall patterns. As hypothesized, DWI path length positively predicted N1 latency (R2 = 0.81, β = 1.51, p = 4.76e-16) and negatively predicted N1 voltage (R2 = 0.79, β = -0.094, p = 9.30e-15), while FA predicted N1 propagation velocity (R2 = 0.35, β = 48.0, p = 0.001).ConclusionWe have demonstrated that the strength and timing of the CCEP N1 is dependent on the properties of the underlying white matter network. Integrated CCEP and DWI visualization allows robust localization of intact axonal pathways which effectively interconnect eloquent cortex.

Project description:IntroductionDiffusion-weighted magnetic resonance imaging (DW-MRI) allows noninvasive investigation of brain structure in vivo. Diffusion tensor imaging (DTI) is a frequently used application of DW-MRI that assumes a single main diffusion direction per voxel, and is therefore not well suited for reconstructing crossing fiber tracts. Among the solutions developed to overcome this problem, constrained spherical deconvolution with probabilistic tractography (CSD-PT) has provided superior quality results in clinical settings on adult subjects; however, it requires particular acquisition parameters and long sequences, which may limit clinical usage in the pediatric age group. The aim of this work was to compare the results of DTI with those of track density imaging (TDI) maps and CSD-PT on data from neonates and children, acquired with low angular resolution and low b-value diffusion sequences commonly used in pediatric clinical MRI examinations.Materials and methodsWe analyzed DW-MRI studies of 50 children (eight neonates aged 3-28?days, 20 infants aged 1-8?months, and 22 children aged 2-17?years) acquired on a 1.5?T Philips scanner using 34 gradient directions and a b-value of 1,000?s/mm2. Other sequence parameters included 60 axial slices; acquisition matrix, 128?×?128; average scan time, 5:34?min; voxel size, 1.75?mm?×?1.75?mm?×?2?mm; one b?=?0 image. For each subject, we computed principal eigenvector (EV) maps and directionally encoded color TDI maps (DEC-TDI maps) from whole-brain tractograms obtained with CSD-PT; the cerebellar-thalamic, corticopontocerebellar, and corticospinal tracts were reconstructed using both CSD-PT and DTI. Results were compared by two neuroradiologists using a 5-point qualitative score.ResultsThe DEC-TDI maps obtained presented higher anatomical detail than EV maps, as assessed by visual inspection. In all subjects, white matter (WM) tracts were successfully reconstructed using both tractography methodologies. The mean qualitative scores of all tracts obtained with CSD-PT were significantly higher than those obtained with DTI (p-value?<?0.05 for all comparisons).ConclusionCSD-PT can be successfully applied to DW-MRI studies acquired at 1.5?T with acquisition parameters adapted for pediatric subjects, thus providing TDI maps with greater anatomical detail. This methodology yields satisfactory results for clinical purposes in the pediatric age group.

Dataset Information

A Direct Cortico-Nigral Pathway as Revealed by Constrained Spherical Deconvolution Tractography in Humans.

Publications

A Direct Cortico-Nigral Pathway as Revealed by Constrained Spherical Deconvolution Tractography in Humans.

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