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John C. Gore

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44

YNICL Journal 2025 Journal Article

Correspondence between thalamic injury-induced changes in resting-state fMRI of monkeys and their sensorimotor behaviors and neural activities

  • Anirban Sengupta
  • Pai-Feng Yang
  • Jamie L. Reed
  • Arabinda Mishra
  • Feng Wang
  • Isaac V Manzanera Esteve
  • Zhangyan Yang
  • Li Min Chen

Resting state functional MRI (rsfMRI) exploits variations in blood-oxygenation-level-dependent (BOLD) signals to infer resting state functional connectivity (FC) within and between brain networks. However, there have been few reports quantifying and validating the results of rsfMRI analyses with other metrics of brain circuits. We measured longitudinal changes in FC both within and between brain networks in three squirrel monkeys after focal lesions of the thalamic ventroposterior lateral nucleus (VPL) that were intended to disrupt the input to somatosensory cortex and impair manual dexterity. Local field potential signals were recorded to assess electrophysiological changes during each animal's recovery, and behavioral performances were measured longitudinally using a sugar-pellet grasping task. Finally, end-point histological evaluations were performed on brain tissue slices to quantify the VPL damage. The rsfMRI data analysis showed significant decrease in FC measures both within and between networks immediately post-injury, which started to recover at different time-points for each animal. The trajectories of FC recovery for each animal mirrored their individual behavioral recovery time-courses. Electrophysiological measurements of inter-electrode coherences and end-point histological measures also aligned well with the graded injury effects measured using rsfMRI-based FC. A simple algorithm employing FC measures from the somatosensory network could accurately predict each monkeys' behavioral recovery timeframe after four weeks post-injury. Whole brain between-network FC measures further revealed that the injury effects were not limited to thalamocortical connections but were rather more widespread. Overall, this study provides evidence of the validity of rsfMRI based FC measures as indicators of the functional integrity and behavioral relevance following an injury to a specific brain circuit.

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YNIMG Journal 2023 Journal Article

Functional alterations in bipartite network of white and grey matters during aging

  • Yurui Gao
  • Yu Zhao
  • Muwei Li
  • Richard D. Lawless
  • Kurt G. Schilling
  • Lyuan Xu
  • Andrea T. Shafer
  • Lori L. Beason-Held

The effects of normal aging on functional connectivity (FC) within various brain networks of gray matter (GM) have been well-documented. However, the age effects on the networks of FC between white matter (WM) and GM, namely WM-GM FC, remains unclear. Evaluating crucial properties, such as global efficiency (GE), for a WM-GM FC network poses a challenge due to the absence of closed triangle paths which are essential for assessing network properties in traditional graph models. In this study, we propose a bipartite graph model to characterize the WM-GM FC network and quantify these challenging network properties. Leveraging this model, we assessed the WM-GM FC network properties at multiple scales across 1,462 cognitively normal subjects aged 22-96 years from three repositories (ADNI, BLSA and OASIS-3) and investigated the age effects on these properties throughout adulthood and during late adulthood (age ≥70 years). Our findings reveal that (1) heterogeneous alterations occurred in region-specific WM-GM FC over the adulthood and decline predominated during late adulthood; (2) the FC density of WM bundles engaged in memory, executive function and processing speed declined with age over adulthood, particularly in later years; and (3) the GE of attention, default, somatomotor, frontoparietal and limbic networks reduced with age over adulthood, and GE of visual network declined during late adulthood. These findings provide unpresented insights into multi-scale alterations in networks of WM-GM functional synchronizations during normal aging. Furthermore, our bipartite graph model offers an extendable framework for quantifying WM-engaged networks, which may contribute to a wide range of neuroscience research.

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YNICL Journal 2023 Journal Article

R1ρ dispersion in white matter correlates with quantitative metrics of cognitive impairment

  • Fatemeh Adelnia
  • Larry T. Davis
  • Lealani Mae Acosta
  • Amanda Puckett
  • Feng Wang
  • Zhongliang Zu
  • Kevin D. Harkins
  • John C. Gore

Much previous neuroimaging research in Alzheimer’s disease has focused on the roles of amyloid and tau proteins, but recent studies have implicated microvascular changes in white matter as early indicators of damage related to later dementia. We used MRI to derive novel, non-invasive measurements of R1ρ dispersion using different locking fields to characterize variations of microvascular structure and integrity in brain tissues. We developed a non-invasive 3D R1ρ dispersion imaging technique using different locking fields at 3T. We acquired MR images and cognitive assessments of participants with mild cognitive impairment (MCI) and compared them to age-matched healthy controls in a cross-sectional study. After providing informed consent, 40 adults aged 62 to 82 years (n = 17 MCI) were included in this study. White matter ΔR1ρ-fraction measured by R1ρ dispersion imaging showed a strong correlation with the cognitive status of older adults (βstd = −0. 4, p-value < 0. 01) independent of age, in contrast to other conventional MRI markers such as T2, R1ρ, and white matter hyperintense lesion volume (WMHs) measured with T2-FLAIR. The correlation of WMHs with cognitive status was no longer significant after adjusting for age and sex in linear regression analysis, and the size of the regression coefficient was substantially decreased (53% lower). This work establishes a new non-invasive method that potentially characterizes impairment of the microvascular structure of white matter in MCI patients compared to healthy controls. The application of this method in longitudinal studies would improve our fundamental understanding of the pathophysiologic changes that accompany abnormal cognitive decline with aging and help identify potential targets for treatment of Alzheimer's disease.

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YNIMG Journal 2022 Journal Article

Detection of functional activity in brain white matter using fiber architecture informed synchrony mapping

  • Yu Zhao
  • Yurui Gao
  • Zhongliang Zu
  • Muwei Li
  • Kurt G. Schilling
  • Adam W. Anderson
  • Zhaohua Ding
  • John C. Gore

A general linear model is widely used for analyzing fMRI data, in which the blood oxygenation-level dependent (BOLD) signals in gray matter (GM) evoked in response to neural stimulation are modeled by convolving the time course of the expected neural activity with a canonical hemodynamic response function (HRF) obtained a priori. The maps of brain activity produced reflect the magnitude of local BOLD responses. However, detecting BOLD signals in white matter (WM) is more challenging as the BOLD signals are weaker and the HRF is different, and may vary more across the brain. Here we propose a model-free approach to detect changes in BOLD signals in WM by measuring task-evoked increases of BOLD signal synchrony in WM fibers. The proposed approach relies on a simple assumption that, in response to a functional task, BOLD signals in relevant fibers are modulated by stimulus-evoked neural activity and thereby show greater synchrony than when measured in a resting state, even if their magnitudes do not change substantially. This approach is implemented in two technical stages. First, for each voxel a fiber-architecture-informed spatial window is created with orientation distribution functions constructed from diffusion imaging data. This provides the basis for defining neighborhoods in WM that share similar local fiber architectures. Second, a modified principal component analysis (PCA) is used to estimate the synchrony of BOLD signals in each spatial window. The proposed approach is validated using a 3T fMRI dataset from the Human Connectome Project (HCP) at a group level. The results demonstrate that neural activity can be reliably detected as increases in fMRI signal synchrony within WM fibers that are engaged in a task with high sensitivities and reproducibility.

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YNIMG Journal 2022 Journal Article

Dynamic variations of resting-state BOLD signal spectra in white matter

  • Muwei Li
  • Yurui Gao
  • Adam W. Anderson
  • Zhaohua Ding
  • John C. Gore

Recent studies have demonstrated that the mathematical model used for analyzing and interpreting fMRI data in gray matter (GM) is inappropriate for detecting or describing blood-oxygenation-level-dependent (BOLD) signals in white matter (WM). In particular the hemodynamic response function (HRF) which serves as the regressor in general linear models is different in WM compared to GM. We recently reported measurements of the frequency contents of resting-state signal time courses in WM that showed distinct power spectra which depended on local structural-vascular-functional associations. In addition, multiple studies of GM have revealed how functional connectivity between regions, as measured by the correlation between BOLD time series, varies dynamically over time. We therefore investigated whether and how BOLD signals from WM in a resting state varied over time. We measured voxel-wise spectrograms, which reflect the time-varying spectral patterns of WM time courses. The results suggest that the spectral patterns are non-stationary but could be categorized into five modes that recurred over time. These modes showed distinct spatial distributions of their occurrences and durations, and the distributions were highly consistent across individuals. In addition, one of the modes exhibited a strong coupling of its occurrence between GM and WM across individuals, and two communities of WM voxels were identified according to the hierarchical structures of transitions among modes. Moreover, these modes are coupled to the shape of instantaneous HRFs. Our findings extend previous studies and reveal the non-stationary nature of spectral patterns of BOLD signals over time, providing a spatial-temporal-frequency characterization of resting-state signals in WM.

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YNICL Journal 2022 Journal Article

Functional connectivity in the dorsal network of the cervical spinal cord is correlated with diffusion tensor imaging indices in relapsing-remitting multiple sclerosis

  • Anna J.E. Combes
  • Kristin P. O'Grady
  • Baxter P. Rogers
  • Kurt G. Schilling
  • Richard D. Lawless
  • Mereze Visagie
  • Delaney Houston
  • Logan Prock

Focal lesions may affect functional connectivity (FC) of the ventral and dorsal networks in the cervical spinal cord of people with relapsing-remitting multiple sclerosis (RRMS). Resting-state FC can be measured using functional MRI (fMRI) at 3T. This study sought to determine whether alterations in FC may be related to the degree of damage in the normal-appearing tissue. Tissue integrity and FC in the cervical spinal cord were assessed with diffusion tensor imaging (DTI) and resting-state fMRI, respectively, in a group of 26 RRMS participants with high cervical lesion load, low disability, and minimally impaired sensorimotor function, and healthy controls. Lower fractional anisotropy (FA) and higher radial diffusivity (RD) were observed in the normal-appearing white matter in the RRMS group relative to controls. Average FC in ventral and dorsal networks was similar between groups. Significant associations were found between higher FC in the dorsal sensory network and several DTI markers of pathology in the normal-appearing tissue. In the normal-appearing grey matter, dorsal FC was positively correlated with axial diffusivity (AD) (r = 0.46, p = 0.020) and mean diffusivity (MD) (r = 0.43, p = 0.032). In the normal-appearing white matter, dorsal FC was negatively correlated with FA (r = -0.43, p = 0.028) and positively correlated with RD (r = 0.49, p = 0.012), AD (r = 0.42, p = 0.037) and MD (r = 0.53, p = 0.006). These results suggest that increased connectivity, while remaining within the normal range, may represent a compensatory mechanism in response to structural damage in support of preserved sensory function in RRMS.

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YNIMG Journal 2021 Journal Article

Functional networks in non-human primate spinal cord and the effects of injury

  • Anirban Sengupta
  • Arabinda Mishra
  • Feng Wang
  • Muwei Li
  • Pai-Feng Yang
  • Li Min Chen
  • John C. Gore

Spontaneous fluctuations of Blood Oxygenation-Level Dependent (BOLD) MRI signal in a resting state have previously been detected and analyzed to describe intrinsic functional networks in the spinal cord of rodents, non-human primates and human subjects. In this study we combined high resolution imaging at high field with data-driven Independent Component Analysis (ICA) to i) delineate fine-scale functional networks within and between segments of the cervical spinal cord of monkeys, and also to ii) characterize the longitudinal effects of a unilateral dorsal column injury on these networks. Seven distinct functional hubs were revealed within each spinal segment, with new hubs detected at bilateral intermediate and gray commissure regions in addition to the bilateral dorsal and ventral horns previously reported. Pair-wise correlations revealed significantly stronger connections between hubs on the dominant hand side. Unilateral dorsal-column injuries disrupted predominantly inter-segmental rather than intra-segmental functional connectivities as revealed by correlation strengths and graph-theory based community structures. The effects of injury on inter-segmental connectivity were evident along the length of the cord both below and above the lesion region. Connectivity strengths recovered over time and there was revival of inter-segmental communities as animals recovered function. BOLD signals of frequency 0.01-0.033 Hz were found to be most affected by injury. The results in this study provide new insights into the intrinsic functional architecture of spinal cord and underscore the potential of functional connectivity measures to characterize changes in networks after an injury and during recovery.

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YNICL Journal 2021 Journal Article

Sensitivity and specificity of CEST and NOE MRI in injured spinal cord in monkeys

  • Feng Wang
  • Zhongliang Zu
  • Tung-Lin Wu
  • Xinqiang Yan
  • Ming Lu
  • Pai-Feng Yang
  • Nellie E. Byun
  • Jamie L. Reed

PURPOSE: , semi-solid magnetization transfer, and direct saturation of free water (DS), were investigated. The overall goal is to develop a protocol for rapid data acquisition for assessing the molecular signatures of the injured spinal cord and its surrounding regions. METHODS: ) method was also used to correct for non-specific factors in quantifying regional spectra around lesion sites. RESULTS: of cysts and other abnormal tissues at and around the lesion site also exhibited significant changes, especially at 3.5, -1.6 and -3.5 ppm RF offsets. CONCLUSION: correction improved the accuracy of CEST and NOE measures. The results provide a rapid (~13 mins), sensitive, and accurate protocol for deriving multiple NOE and CEST effects simultaneously in spinal cord imaging at high field.

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YNIMG Journal 2020 Journal Article

Concomitant modulation of BOLD responses in white matter pathways and cortex

  • Arabinda Mishra
  • Muwei Li
  • Adam W. Anderson
  • Allen T. Newton
  • Zhaohua Ding
  • John C. Gore

In response to a flickering visual stimulus, the BOLD response in primary visual cortex varies with the flickering frequency and is maximal when it is close to 8Hz. In previous studies we demonstrated that BOLD signals in specific white matter (WM) pathways covary with the alternations between stimulus conditions in a block design in similar manner to gray matter (GM) regions. Here we investigated whether WM tracts show varying responses to changes in flicker frequency and are modulated in the same manner as cortical areas. We used a Fourier analysis of BOLD signals to measure the signal amplitude and phase at the fundamental frequency of a block-design task in which flickering visual stimuli alternated with blank presentations, avoiding the assumption of any specific hemodynamic response function. The BOLD responses in WM pathways and the primary visual cortex were evaluated for flicker frequencies varying between 2 and 14Hz. The variations with frequency of BOLD signals in specific WM tracts followed closely those in primary visual cortex, suggesting that variations in cortical activation are directly coupled to corresponding BOLD signals in connected WM tracts. Statistically significant differences in the timings of BOLD responses were also measured between visual cortex and specific WM bundles. These results confirm that when cortical BOLD responses are modulated by selecting different task parameters, relevant WM tracts exhibit corresponding BOLD signals that are also affected.

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YNIMG Journal 2020 Journal Article

Detection of functional networks within white matter using independent component analysis

  • Yali Huang
  • Yang Yang
  • Lei Hao
  • Xuefang Hu
  • Peiguang Wang
  • Zhaohua Ding
  • Jia-Hong Gao
  • John C. Gore

Spontaneous fluctuations in MRI signals from gray matter (GM) in the brain are interpreted as originating from variations in neural activity, and their inter-regional correlations may be analyzed to reveal functional connectivity. However, most studies of intrinsic neuronal activity have ignored the spontaneous fluctuations that also arise in white matter (WM). In this work, we explore spontaneous fluctuations in resting state MRI signals in WM based on spatial independent component analyses (ICA), a data-driven approach that separates signals into independent sources without making specific modeling assumptions. ICA has become widely accepted as a valuable approach for identifying functional connectivity within cortex but has been rarely applied to derive equivalent structures within WM. Here, BOLD signal changes in WM of a group of subjects performing motor tasks were first detected using ICA, and a spatial component whose time course was consistent with the task was found, demonstrating the analysis is sensitive to evoked BOLD signals in WM. Secondly, multiple spatial components were derived by applying ICA to identify those voxels in WM whose MRI signals showed similar temporal behaviors in a resting state. These functionally-related structures are grossly symmetric and coincide with corresponding tracts identified from diffusion MRI. Finally, functional connectivity was quantified by calculating correlations between pairs of structures to explore the synchronicity of resting state BOLD signals across WM regions, and the experimental results revealed that there exist two distinct groupings of functional correlations in WM tracts at rest. Our study provides further insights into the nature of activation patterns, functional responses and connectivity in WM, and support previous suggestions that BOLD signals in WM show similarities with cortical activations and are characterized by distinct underlying structures in tasks and at rest.

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YNIMG Journal 2020 Journal Article

Functional engagement of white matter in resting-state brain networks

  • Muwei Li
  • Yurui Gao
  • Fei Gao
  • Adam W. Anderson
  • Zhaohua Ding
  • John C. Gore

The topological characteristics of functional networks, derived from measurements of resting-state connectivity in gray matter (GM), are associated with individual cognitive abilities or specific dysfunctions. However, blood oxygen level-dependent (BOLD) signals in white matter (WM) are usually ignored or even regressed out as nuisance factors in the data analyses that underlie network models. Recent studies have demonstrated reliable detection of WM BOLD signals and imply these reflect associated neural activities. Here we evaluate quantitatively the contributions of individual WM voxels to the identification of functional networks, which we term their engagement (or conceptually, their importance). We quantify the engagement by measuring the reductions of connectivity, produced by ignoring the signal fluctuations within each WM voxel, with respect to both the entire network (global) or a single GM node (local). We observed highly reproducible spatial distributions of global engagement maps, as well as a trend toward increased relevance of deep WM voxels at delayed times. Local engagement maps exhibit homogeneous spatial distributions with respect to internal nodes that constitute a well-recognized sub-functional network, but inhomogeneous distributions with respect to other nodes. WM voxels show distinct distributions of engagement depending on their anatomical locations. These findings demonstrate the important role of WM in network modeling, thus supporting the need for changes of conventional views that WM signal variations represent only physiological noise.

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YNIMG Journal 2019 Journal Article

Resting-state white matter-cortical connectivity in non-human primate brain

  • Tung-Lin Wu
  • Feng Wang
  • Muwei Li
  • Kurt G. Schilling
  • Yurui Gao
  • Adam W. Anderson
  • Li Min Chen
  • Zhaohua Ding

Numerous studies have used functional magnetic resonance imaging (fMRI) to characterize functional connectivity between cortical regions by analyzing correlations in blood oxygenation level dependent (BOLD) signals in a resting state. However, to date, there have been only a handful of studies reporting resting state BOLD signals in white matter. Nonetheless, a growing number of reports has emerged in recent years suggesting white matter BOLD signals can be reliably detected, though their biophysical origins remain unclear. Moreover, recent studies have identified robust correlations in a resting state between signals from cortex and specific white matter tracts. In order to further validate and interpret these findings, we studied a non-human primate model to investigate resting-state connectivity patterns between parcellated cortical volumes and specific white matter bundles. Our results show that resting-state connectivity patterns between white and gray matter structures are not randomly distributed but share notable similarities with diffusion- and histology-derived anatomic connectivities. This suggests that resting-state BOLD correlations between white matter fiber tracts and the gray matter regions to which they connect are directly related to the anatomic arrangement and density of WM fibers. We also measured how different levels of baseline neural activity, induced by varying levels of anesthesia, modulate these patterns. As anesthesia levels were raised, we observed weakened correlation coefficients between specific white matter tracts and gray matter regions while key features of the connectivity pattern remained similar. Overall, results from this study provide further evidence that neural activity is detectable by BOLD fMRI in both gray and white matter throughout the resting brain. The combined use of gray and white matter functional connectivity could also offer refined full-scale functional parcellation of the entire brain to characterize its functional architecture.

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YNICL Journal 2019 Journal Article

Spatiotemporal trajectories of quantitative magnetization transfer measurements in injured spinal cord using simplified acquisitions

  • Feng Wang
  • Tung-Lin Wu
  • Ke Li
  • Li Min Chen
  • John C. Gore

PURPOSE: This study aims to systematically evaluate the accuracy and precision of pool size ratio (PSR) measurements from quantitative magnetization transfer (qMT) acquisitions using simplified models in the context of assessing injury-associated spatiotemporal changes in spinal cords of non-human primates. This study also aims to characterize changes in the spinal tissue pathology in individual subjects, both regionally and longitudinally, in order to demonstrate the relationship between regional tissue compositional changes and sensorimotor behavioral recovery after cervical spinal cord injury (SCI). METHODS: MRI scans were recorded on anesthetized monkeys at 9.4 T, before and serially after a unilateral section of the dorsal column tract. Images were acquired following saturating RF pulses at different offset frequencies. Models incorporating two pools of protons but with differing numbers of variable parameters were used to fit the data to derive qMT parameters. The results using different amounts of measured data and assuming different numbers of variable model parameters were compared. Behavioral impairments and recovery were assessed by a food grasping-retrieving task. Histological sections were obtained post mortem for validation of the injury. RESULTS: QMT fitting provided maps of pool size ratio (PSR), the relative amounts of immobilized protons exchanging magnetization compared to the "free" water. All the selected modeling approaches detected a lesion/cyst at the site of injury as significant reductions in PSR values. The regional contrasts in the PSR maps obtained using the different fittings varied, but the 2-parameter fitting results showed strong positive correlations with results from 5-parameter modeling. 2-parameter fitting results with modest (>3) RF offsets showed comparable sensitivity for detecting demyelination in white matter and loss of macromolecules in gray matter around lesion sites compared to 5-parameter fitting with fully-sampled data acquisitions. Histology confirmed that decreases of PSR corresponded to regional demyelination around lesion sites, especially when demyelination occurred along the dorsal column on the injury side. Longitudinally, PSR values of injured dorsal column tract and gray matter horns exhibited remarkable recovery that associated with behavioral improvement. CONCLUSION: Simplified qMT modeling approaches provide efficient and sensitive means to detect and characterize injury-associated demyelination in white matter tracts and loss of macromolecules in gray matter and to monitor its recovery over time.

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YNIMG Journal 2018 Journal Article

Spinal cord MRI at 7T

  • Robert L. Barry
  • S. Johanna Vannesjo
  • Samantha By
  • John C. Gore
  • Seth A. Smith

Magnetic resonance imaging (MRI) of the human spinal cord at 7T has been demonstrated by a handful of research sites worldwide, and the spinal cord remains one of the areas in which higher fields and resolution could have high impact. The small diameter of the cord (∼1 cm) necessitates high spatial resolution to minimize partial volume effects between gray and white matter, and so MRI of the cord can greatly benefit from increased signal-to-noise ratio and contrasts at ultra-high field (UHF). Herein we review the current state of UHF spinal cord imaging. Technical challenges to successful UHF spinal cord MRI include radiofrequency (B1) nonuniformities and a general lack of optimized radiofrequency coils, amplified physiological noise, and an absence of methods for robust B0 shimming along the cord to mitigate image distortions and signal losses. Numerous solutions to address these challenges have been and are continuing to be explored, and include novel approaches for signal excitation and acquisition, dynamic shimming and specialized shim coils, and acquisitions with increased coverage or optimal slice angulations.

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YNIMG Journal 2018 Journal Article

Voxel-wise detection of functional networks in white matter

  • Yali Huang
  • Stephen K. Bailey
  • Peiguang Wang
  • Laurie E. Cutting
  • John C. Gore
  • Zhaohua Ding

Functional magnetic resonance imaging (fMRI) depicts neural activity in the brain indirectly by measuring blood oxygenation level dependent (BOLD) signals. The majority of fMRI studies have focused on detecting cortical activity in gray matter (GM), but whether functional BOLD signal changes also arise in white matter (WM), and whether neural activities trigger hemodynamic changes in WM similarly to GM, remain controversial, particularly in light of the much lower vascular density in WM. However, BOLD effects in WM are readily detected under hypercapnic challenges, and the number of reports supporting reliable detections of stimulus-induced activations in WM continues to grow. Rather than assume a particular hemodynamic response function, we used a voxel-by-voxel analysis of frequency spectra in WM to detect WM activations under visual stimulation, whose locations were validated with fiber tractography using diffusion tensor imaging (DTI). We demonstrate that specific WM regions are robustly activated in response to visual stimulation, and that regional distributions of WM activation are consistent with fiber pathways reconstructed using DTI. We further examined the variation in the concordance between WM activation and fiber density in groups of different sample sizes, and compared the signal profiles of BOLD time series between resting state and visual stimulation conditions in activated GM as well as activated and non-activated WM regions. Our findings confirm that BOLD signal variations in WM are modulated by neural activity and are detectable with conventional fMRI using appropriate methods, thus offering the potential of expanding functional connectivity measurements throughout the brain.

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YNIMG Journal 2017 Journal Article

Functional connectivity and activity of white matter in somatosensory pathways under tactile stimulations

  • Xi Wu
  • Zhipeng Yang
  • Stephen K. Bailey
  • Jiliu Zhou
  • Laurie E. Cutting
  • John C. Gore
  • Zhaohua Ding

Functional MRI has proven to be effective in detecting neural activity in brain cortices on the basis of blood oxygenation level dependent (BOLD) contrast, but has relatively poor sensitivity for detecting neural activity in white matter. To demonstrate that BOLD signals in white matter are detectable and contain information on neural activity, we stimulated the somatosensory system and examined distributions of BOLD signals in related white matter pathways. The temporal correlation profiles and frequency contents of BOLD signals were compared between stimulation and resting conditions, and between relevant white matter fibers and background regions, as well as between left and right side stimulations. Quantitative analyses show that, overall, MR signals from white matter fiber bundles in the somatosensory system exhibited significantly greater temporal correlations with the primary sensory cortex and greater signal power during tactile stimulations than in a resting state, and were stronger than corresponding measurements for background white matter both during stimulations and in a resting state. The temporal correlation and signal power under stimulation were found to be twice those observed from the same bundle in a resting state, and bore clear relations with the side of stimuli. These indicate that BOLD signals in white matter fibers encode neural activity related to their functional roles connecting cortical volumes, which are detectable with appropriate methods.

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YNIMG Journal 2016 Journal Article

Reproducibility of resting state spinal cord networks in healthy volunteers at 7 Tesla

  • Robert L. Barry
  • Baxter P. Rogers
  • Benjamin N. Conrad
  • Seth A. Smith
  • John C. Gore

We recently reported our findings of resting state functional connectivity in the human spinal cord: in a cohort of healthy volunteers we observed robust functional connectivity between left and right ventral (motor) horns and between left and right dorsal (sensory) horns (Barry et al. , 2014). Building upon these results, we now quantify the within-subject reproducibility of bilateral motor and sensory networks (intraclass correlation coefficient=0. 54–0. 56) and explore the impact of including frequencies up to 0. 13Hz. Our results suggest that frequencies above 0. 08Hz may enhance the detectability of these resting state networks, which would be beneficial for practical studies of spinal cord functional connectivity.

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YNIMG Journal 2014 Journal Article

Mapping mean axon diameter and axonal volume fraction by MRI using temporal diffusion spectroscopy

  • Junzhong Xu
  • Hua Li
  • Kevin D. Harkins
  • Xiaoyu Jiang
  • Jingping Xie
  • Hakmook Kang
  • Mark D. Does
  • John C. Gore

Mapping mean axon diameter and intra-axonal volume fraction may have significant clinical potential because nerve conduction velocity is directly dependent on axon diameter, and several neurodegenerative diseases affect axons of specific sizes and alter axon counts. Diffusion-weighted MRI methods based on the pulsed gradient spin echo (PGSE) sequence have been reported to be able to assess axon diameter and volume fraction non-invasively. However, due to the relatively long diffusion times used, e. g. >20ms, the sensitivity to small axons (diameter<2μm) is low, and the derived mean axon diameter has been reported to be overestimated. In the current study, oscillating gradient spin echo (OGSE) diffusion sequences with variable frequency gradients were used to assess rat spinal white matter tracts with relatively short effective diffusion times (1–5ms). In contrast to previous PGSE-based methods, the extra-axonal diffusion cannot be modeled as hindered (Gaussian) diffusion when short diffusion times are used. Appropriate frequency-dependent rates are therefore incorporated into our analysis and validated by histology-based computer simulation of water diffusion. OGSE data were analyzed to derive mean axon diameters and intra-axonal volume fractions of rat spinal white matter tracts (mean axon diameter of ~1. 27–5. 54μm). The estimated values were in good agreement with histology, including the small axon diameters (<2. 5μm). This study establishes a framework for the quantification of nerve morphology using the OGSE method with high sensitivity to small axons.

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YNICL Journal 2013 Journal Article

Identification of promethazine as an amyloid-binding molecule using a fluorescence high-throughput assay and MALDI imaging mass spectrometry

  • Richard A. McClure
  • Chad W. Chumbley
  • Michelle L. Reyzer
  • Kevin Wilson
  • Richard M. Caprioli
  • John C. Gore
  • Wellington Pham

The identification of amyloid-binding compounds is a crucial step in the development of imaging probes and therapeutics for the detection and cure of Alzheimer's disease. Unfortunately, the process typically lags during the translation from in vitro to in vivo studies due to the impenetrable nature of the blood brain barrier (BBB). Here, we integrate fluorescence assay with MALDI imaging mass spectrometry to screen known compounds and repurpose their properties to enable the second function of binding to amyloid plaques. Through this approach, we identified an antihistamine compound, promethazine, that can bind to amyloid plaques. Finally, we demonstrate that promethazine is retained in the amyloid-burdened brain compared to a normal brain and that its distribution within the brain corroborates with that of amyloid plaques.

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YNIMG Journal 2013 Journal Article

Layer-specific BOLD activation in awake monkey V1 revealed by ultra-high spatial resolution functional magnetic resonance imaging

  • Gang Chen
  • Feng Wang
  • John C. Gore
  • Anna W. Roe

The laminar structure of the cortex has previously been explored both in non-human primates and human subjects using high-resolution functional magnetic resonance imaging (fMRI). However, whether the spatial specificity of the blood-oxygenation-level-dependent (BOLD) fMRI is sufficiently high to reveal lamina specific organization in the cortex reliably is still unclear. In this study we demonstrate for the first time the detection of such layer-specific activation in awake monkeys at the spatial resolution of 200×200×1000μm3 in a vertical 4. 7T scanner. Results collected in trained monkeys are high in contrast-to-noise ratio and low in motion artifacts. Isolation of laminar activation was aided by choosing the optimal slice orientation and thickness using a novel pial vein pattern analysis derived from optical imaging. We found that the percent change of GE-BOLD signal is the highest at a depth corresponding to layer IV. Changes in the middle layers (layer IV) were 30% greater than changes in the top layers (layers I–III), and 32% greater than the bottom layers (layers V/VI). The laminar distribution of BOLD signal correlates well with neural activity reported in the literature. Our results suggest that the high intrinsic spatial resolution of GE-BOLD signal is sufficient for mapping sub-millimeter functional structures in awake monkeys. This degree of spatial specificity will be useful for mapping both laminar activations and columnar structures in the cerebral cortex.

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YNIMG Journal 2013 Journal Article

Measuring relative timings of brain activities using fMRI

  • Santosh B. Katwal
  • John C. Gore
  • J. Christopher Gatenby
  • Baxter P. Rogers

Functional MRI (fMRI) has previously been shown to be able to measure hundreds of milliseconds differences in timings of activities in different brain regions, even though the underlying blood oxygenation level-dependent (BOLD) response is delayed and dispersed on the order of seconds. This capability may contribute towards the study of communication within the brain by assessing the temporal sequences of various brain processes (mental chronometry). The practical limit of fMRI for detecting the relative timing of brain activity is not known. We aimed to detect fine differences in the timings of brain activities beyond those previously measured from fMRI data in human subjects. We introduced known delays between the onsets of visual stimuli in a controlled, sparse event-related design and investigated if the temporal shifts in the corresponding average BOLD signals were detectable. To maximize sensitivity, we used high spatial and temporal resolution fMRI at ultrahigh field (7 T), in conjunction with a novel data-driven technique for voxel selection using graph-based visualizations of self-organizing maps and Granger causality to measure relative timing. This approach detected timing differences as small as 28ms in visual cortex in individual subjects. For signal extraction, the self-organizing map approach outperformed other common techniques including independent component analysis, voxelwise univariate linear regression analysis and a separate localizer scan. For relative timing measurement, Granger causality outperformed time-to-peak calculations derived from an inverse logit curve fit. We conclude that high-resolution imaging at ultrahigh field, signal extraction via self-organizing map, and appropriate use of Granger causality permit the detection of small timing differences in fMRI data, despite the intrinsically slow hemodynamic response.

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YNIMG Journal 2013 Journal Article

Quantitative magnetization transfer imaging of human brain at 7 T

  • Richard D. Dortch
  • Jay Moore
  • Ke Li
  • Marcin Jankiewicz
  • Daniel F. Gochberg
  • Jane A. Hirtle
  • John C. Gore
  • Seth A. Smith

Quantitative magnetization transfer (qMT) imaging yields indices describing the interactions between free water protons and immobile macromolecular protons. These indices include the macromolecular to free pool size ratio (PSR), which has been shown to be correlated with myelin content in white matter. Because of the long scan times required for whole-brain imaging (≈20–30min), qMT studies of the human brain have not found widespread application. Herein, we investigated whether the increased signal-to-noise ratio available at 7. 0T could be used to reduce qMT scan times. More specifically, we developed a selective inversion recovery (SIR) qMT imaging protocol with a i) novel transmit radiofrequency (B 1 +) and static field (B 0) insensitive inversion pulse, ii) turbo field-echo readout, and iii) reduced TR. In vivo qMT data were obtained in the brains of healthy volunteers at 7. 0T using the resulting protocol (scan time≈40s/slice, resolution=2×2×3mm3). Reliability was also assessed in repeated acquisitions. The results of this study demonstrate that SIR qMT imaging can be reliably performed within the radiofrequency power restrictions present at 7. 0T, even in the presence of large B 1 + and B 0 inhomogeneities. Consistent with qMT studies at lower field strengths, the observed PSR values were higher in white matter (mean±SD=17. 6±1. 3%) relative to gray matter (10. 3±1. 6%) at 7. 0T. In addition, regional variations in PSR were observed in white matter. Together, these results suggest that qMT measurements are feasible at 7. 0T and may eventually allow for the high-resolution assessment of changes in composition throughout the normal and diseased human brain in vivo.

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YNIMG Journal 2012 Journal Article

Identification of cortical lamination in awake monkeys by high resolution magnetic resonance imaging

  • Gang Chen
  • Feng Wang
  • John C. Gore
  • Anna W. Roe

Brodmann divided the neocortex into 47 different cortical areas based on histological differences in laminar myeloarchitectonic and cytoarchitectonic defined structure. The ability to do so in vivo with anatomical magnetic resonance (MR) methods in awake subjects would be extremely advantageous for many functional studies. However, due to the limitations of spatial resolution and contrast, this has been difficult to achieve in awake subjects. Here, we report that by using a combination of MR microscopy and novel contrast effects, cortical layers can be delineated in the visual cortex of awake subjects (nonhuman primates) at 4. 7T. We obtained data from 30-min acquisitions at voxel size of 62. 5×62. 5×1000μm3 (4nl). Both the phase and magnitude components of the T2*-weighted image were used to generate laminar profiles which are believed to reflect variations in myelin and local cell density content across cortical depth. Based on this, we were able to identify six layers characteristic of the striate cortex (V1). These were the stripe of Kaes-Bechterew (in layer II/III), the stripe of Gennari (in layer IV), the inner band of Baillarger (in layer V), as well as three sub-layers within layer IV (IVa, IVb, and IVc). Furthermore, we found that the laminar structure of two extrastriate visual cortex (V2, V4) can also be detected. Following the tradition of Brodmann, this significant improvement in cortical laminar visualization should make it possible to discriminate cortical regions in awake subjects corresponding to differences in myeloarchitecture and cytoarchitecture.

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YNIMG Journal 2012 Journal Article

Improving measurement of functional connectivity through decreasing partial volume effects at 7T

  • Allen T. Newton
  • Baxter P. Rogers
  • John C. Gore
  • Victoria L. Morgan

Several applications of fMRI at high field have taken advantage of the increased BOLD contrast to increase spatial resolution, but the potential benefits of higher fields for detecting and analyzing functional connectivity have largely been unexplored. We measured the influence of spatial resolution at 7T on estimates of functional connectivity through decreased partial volume averaging. Ten subjects were imaged at 7T with a range of spatial resolutions (1×1×2mm to 3×3×2mm) during performance of a finger tapping task and in the resting state. We found that resting state correlations within the sensory-motor system increase as voxel dimensions decreased from 3×3×2mm to 1×1×2mm, whereas connectivity to other brain regions was unaffected. This improvement occurred even as overall signal to noise ratios decrease. Our data suggest that this increase may be due to decreased partial volume averaging, and that functional connectivity within the primary seed region is heterogeneous on the scale of single voxels.

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YNIMG Journal 2011 Journal Article

Data-driven optimization and evaluation of 2D EPI and 3D PRESTO for BOLD fMRI at 7 Tesla: I. Focal coverage

  • Robert L. Barry
  • Stephen C. Strother
  • J. Christopher Gatenby
  • John C. Gore

Blood oxygenation level dependent (BOLD) functional magnetic resonance imaging (fMRI) is commonly performed using 2D single-shot echo-planar imaging (EPI). However, single-shot EPI at 7 Tesla (T) often suffers from significant geometric distortions (due to low bandwidth (BW) in the phase-encode (PE) direction) and amplified physiological noise. Recent studies have suggested that 3D multi-shot sequences such as PRESTO may offer comparable BOLD contrast-to-noise ratio with increased volume coverage and decreased geometric distortions. Thus, a four-way group-level comparison was performed between 2D and 3D acquisition sequences at two in-plane resolutions. The quality of fMRI data was evaluated via metrics of prediction and reproducibility using NPAIRS (Non-parametric Prediction, Activation, Influence and Reproducibility re-Sampling). Group activation maps were optimized for each acquisition strategy by selecting the number of principal components that jointly maximized prediction and reproducibility, and showed good agreement in sensitivity and specificity for positive BOLD changes. High-resolution EPI exhibited the highest z-scores of the four acquisition sequences; however, it suffered from the lowest BW in the PE direction (resulting in the worst geometric distortions) and limited spatial coverage, and also caused some subject discomfort through peripheral nerve stimulation (PNS). In comparison, PRESTO also had high z-scores (higher than EPI for a matched in-plane resolution), the highest BW in the PE direction (producing images with superior geometric fidelity), the potential for whole-brain coverage, and no reported PNS. This study provides evidence to support the use of 3D multi-shot acquisition sequences in lieu of single-shot EPI for ultra high field BOLD fMRI at 7T.

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YNIMG Journal 2011 Journal Article

Differentiation of somatosensory cortices by high-resolution fMRI at 7 T

  • Elizabeth Ann Stringer
  • Li Min Chen
  • Robert M. Friedman
  • Christopher Gatenby
  • John C. Gore

This study aimed to evaluate the ability of BOLD signals at high MRI field (7T) to map fine-scale single-digit activations in subdivisions (areas 3b and 1) of the human primary somatosensory cortex (SI) in individual subjects. We acquired BOLD fMRI data from cortical areas around the central suclus in six healthy human subjects while stimulating individual finger pads with 2-Hz air puffs. Discrete, single-digit responses were identified in an area along the posterior bank of the central sulcus corresponding to area 3b and in an area along the crest of the postcentral gyrus corresponding to area 1. In single subjects, activations of digits 1 to 4 in both areas 3b and 1 were organized in a somatotopic manner. The separation of digit representations was measured for adjacent digits and was approximately 1. 6 times greater in area 3b than in area 1. Within individual subjects, the cortical responses to single-digit stimulations and the magnitude of the BOLD signals were reproducible across imaging runs and were comparable across subjects. Our findings demonstrate that BOLD fMRI at 7T is capable of revealing the somatotopic organization of single-digit activations with good within-subject reliability and reproducibility, and activation maps can be acquired within a reasonably short time window, which are essential characteristics for several neurological applications within patient populations.

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YNIMG Journal 2006 Journal Article

Connectivity–behavior analysis reveals that functional connectivity between left BA39 and Broca's area varies with reading ability

  • Michelle Hampson
  • Fuyuze Tokoglu
  • Zhongdong Sun
  • Robin J. Schafer
  • Pawel Skudlarski
  • John C. Gore
  • R. Todd Constable

Correlations between temporal fluctuations in MRI signals may reveal functional connectivity between brain regions within individual subjects. Such correlations would be especially useful indices of functional connectivity if they covary with behavioral performance or other subject variables. This study investigated whether such a relationship could be demonstrated in the context of the reading circuit in the brain. The method proved sufficiently powerful to reveal significant correlations between the reading abilities of subjects and the strength of their functional connection between left Brodmann's area 39 and Broca's area during reading. This suggests that the disconnection of the angular gyrus previously reported for dyslexic readers is part of a larger continuum in which poor (but nonimpaired readers) also show reduced connectivity to the region. In addition, it illustrates the potential power of paradigms that examine correlations between behavior and functional brain connections.

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YNIMG Journal 2006 Journal Article

Improved fiber tractography with Bayesian tensor regularization

  • Yonggang Lu
  • Akram Aldroubi
  • John C. Gore
  • Adam W. Anderson
  • Zhaohua Ding

Diffusion tensor tractography suffers from the effects of noise and partial volume averaging (PVA). For reliable reconstruction of fiber pathways, tracking algorithms that are robust to these artifacts are called for. To meet this need, the present study establishes a novel Bayesian regularization framework for fiber tracking that takes into account the effects of noise and PVA, thereby improving tracking accuracy and precision. With this framework, the propagation of a fiber path follows an optimal vector determined by Bayes decision rule; the probability functions involved are modeled on the basis of multivariate normal distributions of diffusion tensor elements, which allows the optimal solution with maximum a posteriori probability to be derived analytically. Parameters for the probability functions are estimated from the uncertainty of tensor elements and the variance among tensors within an oriented sampling volume weighted by fractional anisotropy. Experiments with Monte Carlo simulations, synthetic, and in vivo human diffusion tensor data demonstrate that this specialized scheme enhances the immunity of fiber tracking to noise and PVA, and hence enables fibers to be more faithfully reconstructed.

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YNIMG Journal 2002 Journal Article

Simultaneous Recording of Event-Related Auditory Oddball Response Using Transcranial Near Infrared Optical Topography and Surface EEG

  • Richard P. Kennan
  • Silvina G. Horovitz
  • Atsushi Maki
  • Yuichi Yamashita
  • Hideaki Koizumi
  • John C. Gore

Near infrared optical topography (OT) is the measurement of hemoglobin absorption simultaneously from an array of optical fibers on the scalp to construct maps of cortical activity. We demonstrate that OT can be used to simultaneously detect and characterize the hemodynamic responses associated with an “oddball” auditory stimulus and that corresponding electrical event related potentials can be acquired simultaneously using conventional scalp recordings. In addition to the measured electrical response, the hemodynamic localization is consistent with fMRI studies, which show significant activation in the temporal and parietal cortical regions. The event-related response of total hemoglobin showed relatively slow peak latencies (5. 8 ± 0. 3 s), which were also consistent with fMRI. The current study shows the regions of peak hemodynamic activity that are in closest proximity to areas of peak electrical activity. This is the first demonstration of simultaneous ERP electrical recording and non-invasive optical mapping in human subjects, which promises to be an important tool in the characterization of both normal and abnormal brain function.

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YNIMG Journal 2001 Journal Article

The Functional Neural Architecture of Components of Attention in Language-Processing Tasks

  • Bennett A. Shaywitz
  • Sally E. Shaywitz
  • Kenneth R. Pugh
  • Robert K. Fulbright
  • Pawel Skudlarski
  • W.Einar Mencl
  • R.Todd Constable
  • Karen E. Marchione

Using functional magnetic resonance imaging we examined three important dimensions of attentional control (selective attention, divided attention, and executive function) in 25 neurologically normal, right-handed men and women, using tasks involving the perception and processing of printed words, spoken words, or both. In the context of language-processing manipulations: selective attention resulted in increased activation at left hemisphere parietal sites as well as at inferior frontal sites, divided attention resulted in additional increases in activation at these same left hemisphere sites and was also uniquely associated with increased activation of homologous sites in the right hemisphere, and executive function (measured during a complex task requiring sequential decision-making) resulted in increased activation at frontal sites relative to all other conditions. Our findings provide support for the belief that specific functional aspects of attentional control in language processing involve widely distributed but distinctive cortical systems, with mechanisms associated with the control of perceptual selectivity involving primarily parietal and inferior frontal sites and executive function engaging specific sites in frontal cortex.

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YNIMG Journal 1999 Journal Article

An Event-Related fMRI Study of Implicit Phrase-Level Syntactic and Semantic Processing

  • A.Min Kang
  • R.Todd Constable
  • John C. Gore
  • Sergey Avrutin

Most neuroimaging studies of language function to date use a block-subtraction paradigm in which images acquired during relatively long periods of target stimuli are compared to those acquired during a control period. These studies typically require an overt response on the part of the subject, usually some type of discrimination or grammatical judgment by button press, or silent word generation. Results from studies of syntactic and semantic processing have generally been compatible with the classical correlation to Broca's area and Wernicke's area, respectively. Recently, functional magnetic resonance imaging (fMRI) studies departing from the block-subtraction paradigm in favor of event-related fMRI paradigms have been reported. We have extended the use of this approach to examine implicit (i. e. , without an explicit task on the part of the subject) syntactic and semantic processing at the phrasal level, using visually presented verb phrases. Left BA 44 is more strongly activated for the syntactic condition than the semantic condition. BA 45, 10, and 46 show laterality differences: mostly left-lateralized for the syntactic condition and right-lateralized for the semantic condition. We also find activations of the inferior parietal lobe, consistent with a visual oddball response reported previously, and the anterior cingulate gyrus (BA 32), implicated for attention and memory-related processes in numerous studies.

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YNIMG Journal 1999 Journal Article

ROC Analysis of Statistical Methods Used in Functional MRI: Individual Subjects

  • Pawel Skudlarski
  • R.Todd Constable
  • John C. Gore

The complicated structure of fMRI signals and associated noise sources make it difficult to assess the validity of various steps involved in the statistical analysis of brain activation. Most methods used for fMRI analysis assume that observations are independent and that the noise can be treated as white gaussian noise. These assumptions are usually not true but it is difficult to assess how severely these assumptions are violated and what are their practical consequences. In this study a direct comparison is made between the power of various analytical methods used to detect activations, without reference to estimates of statistical significance. The statistics used in fMRI are treated as metrics designed to detect activations and are not interpreted probabilistically. The receiver operator characteristic (ROC) method is used to compare the efficacy of various steps in calculating an activation map in the study of a single subject based on optimizing the ratio of the number of detected activations to the number of false-positive findings. The main findings are as follows: Preprocessing. The removal of intensity drifts and high-pass filtering applied on the voxel time-course level is beneficial to the efficacy of analysis. Temporal normalization of the global image intensity, smoothing in the temporal domain, and low-pass filtering do not improve power of analysis. Choices of statistics. the cross-correlation coefficient andt-statistic, as well as nonparametric Mann–Whitney statistics, prove to be the most effective and are similar in performance, by our criterion. Task design. the proper design of task protocols is shown to be crucial. In an alternating block design the optimal block length is be approximately 18 s. Spatial clustering. an initial spatial smoothing of images is more efficient than cluster filtering of the statistical parametric activation maps.

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YNIMG Journal 1998 Journal Article

Measurements of the Temporal fMRI Response of the Human Auditory Cortex to Trains of Tones

  • Matthew D. Robson
  • Jennifer L. Dorosz
  • John C. Gore

Averaged single trials (AST) allowed the functional magnetic resonance imaging (fMRI) response to auditory stimuli to be measured at high temporal (1 s) and spatial (0. 1 cm3) resolution. Using this paradigm we investigated the transient signal response to 100-ms tone bursts in trains of between 100 ms and 25. 5 s in total duration. We have demonstrated that the fMRI response to such auditory stimuli is approximately linear for trains of 6 s and longer, but that shorter stimuli produce signals that are larger than might be expected from the response to the longer stimuli. This nonlinear behavior can be modeled if an adaptive response to each stimulus is assumed. A study using a novel paradigm was also performed in order to study the influence of scanner noise during fMRI experiments on the auditory system response to tones. This study demonstrated that the temporal response to 700-ms tone stimuli is modified when performed in the presence of scanner gradient noise, the modification being a small but significant increase (P <0. 05) in the magnitude of the response. Finally the ability to measure the onset of functional activation using the AST method was examined. It was found, with the aid of computer simulation that a sampling rate of one image per second is adequate to distinguish temporal responses. Using the data acquired in this study, onset times were calculated for the auditory cortex, and these results are consistent with current models of functional activation.

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YNIMG Journal 1996 Journal Article

Auditory Selective Attention: An fMRI Investigation

  • Kenneth R. Pugh
  • Bennett A. Shaywitz
  • Sally E. Shaywitz
  • Robert K. Fulbright
  • Dani Byrd
  • Pawel Skudlarski
  • Donald P. Shankweiler
  • Leonard Katz

In the present experiment, 25 adult subjects discriminated speech tokens ([ba]/[da]) or made pitch judgments on tone stimuli (rising/falling) under both binaural and dichotic listening conditions. We observed that when listeners performed tasks under the dichotic conditions, during which greater demands are made on auditory selective attention, activation within the posterior (parietal) attention system and at primary processing sites in the superior temporal and inferior frontal regions was increased. The cingulate gyrus within the anterior attention system was not influenced by this manipulation. Hemispheric differences between speech and nonspeech tasks were also observed, both at Broca's Area within the inferior frontal gyrus and in the middle temporal gyrus.

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