bioRxiv Science⌕ Search

Biology subjects

Boes, A. D.

Publications and source records attributed to Boes, A. D..

14 recordsLinked to original sources

Transcranial magnetic stimulation to the dorsolateral prefrontal cortex modulates single-neuron activity in humans

Transcranial magnetic stimulation (TMS) to the dorsolateral prefrontal cortex (dlPFC) is an FDA-cleared treatment for depression, yet how cortical stimulation influences single neurons in deep brain circuits remains unknown. Using intracranial microelectrode recordings in four neurosurgical patients, we resolved single-neuron spikes as early as 8 ms from 185 single neurons after single-pulse left dlPFC TMS. TMS elicited time-locked firing responses in 46% of neurons across deep cortical and subcortical structures bilaterally. TMS facilitated putative interneuron spiking in striato-thalamic regions from [~]8 ms, peaking at [~]80-100 ms, and lasting to [~]1000 ms, while suppressing putative pyramidal cell spiking with a delayed and slower time course. Trial-by-trial single-neuron modulations were positively correlated with cortico-striato-thalamic network activity and anti-correlated with limbic network activity. These findings reveal that dlPFC TMS facilitates inhibitory firing in executive control networks while suppressing limbic excitatory drive, providing a cellular mechanism for how cortical stimulation modulates distributed brain networks.

neuroscience↗

Distributed neural signatures of discomfort induced by transcranial magnetic stimulation

Transcranial magnetic stimulation (TMS) is a cornerstone tool for causal inference in human brain function and an increasingly used neuromodulation therapy, yet it induces well-recognized discomfort that may systematically bias measured outcomes. Despite its ubiquity, a critical gap remains in understanding how TMS-induced discomfort is represented across the brain and to what extent it contributes to TMS-evoked neural responses. Using concurrent TMS-fMRI across 11 cortical targets, we collected an unprecedented dataset (165 participants; 1,535 runs) spanning healthy participants and those with elevated affective symptoms. Cross-validated multivariate modeling revealed that TMS-induced discomfort engages distributed cortical and subcortical regions across sensorimotor, attentional, default mode, and limbic networks, with both shared and group-specific patterns. Discomfort-related activity accounted for approximately 12% and 25% of TMS-evoked responses in healthy and elevated-symptom groups, respectively, and varied systematically across stimulating sites. These findings identify TMS-induced discomfort as a substantial and previously under-characterized component of TMS-evoked neural responses, underscoring the need to explicitly measure and model it. By providing a whole-brain map of regional contributions associated with TMS-induced discomfort and an analytic framework to dissociate direct neuromodulatory effects from discomfort-related responses, this work improves the interpretability of TMS-evoked signals and supports more rigorous causal inference and therapeutic applications.

neuroscience↗

The methodological foundations of lesion network mapping remain sound

Lesion network mapping (LNM) and related techniques have been used in over 200 studies, primarily to test whether anatomically distributed lesions that cause the same symptom fall within a common brain network. A recent article1 challenges the specificity and validity of this technique, suggesting that lesion network maps primarily reflect intrinsic properties of the normative connectome rather than lesion-symptom relationships. However, the data and procedures in van den Heuvel et al. do not reflect those used in most LNM studies. Further, the main conclusions were based on similarity between maps, but similarity does not imply the absence of meaningful differences. In contrast, LNM provides evidence for meaningful differences using specificity testing. Exemplary analyses of 1090 lesion locations from 34 prior LNM studies do not support van den Heuvels concerns and confirm the lesion-deficit specificity of LNM. While we encourage further methodological investigation, the analyses of van den Heuvel et al. do not invalidate prior LNM findings or future applications.

neuroscience↗

A Practical Preprocessing Pipeline for Concurrent TMS-iEEG: Critical Steps and Methodological Considerations

Transcranial magnetic stimulation combined with intracranial EEG (TMS-iEEG) has emerged as a powerful approach for probing the causal organization and dynamics of the human brain. Despite its promise, the presence of TMS-induced artifacts poses significant challenges for accurately characterizing and interpreting evoked neural responses. In this study, we present a practical preprocessing pipeline for single pulse TMS-iEEG data, incorporating key steps of re-referencing, filtering, artifact interpolation, and detrending. Using both real and simulated data, we systematically evaluated the effects of each step and compared alternative methodological choices. Our results demonstrate that this pipeline effectively attenuated various types of artifacts and noise, yielding cleaner signals for the subsequent analysis of intracranial TMS-evoked potentials (iTEPs). Moreover, we showed that methodological choices can substantially influence iTEPs outcomes. In particular, referencing methods might strongly affect iTEP morphology and amplitude, underscoring the importance of tailoring the referencing strategy to specific signal characteristics and research objectives. For filtering, we recommend a segment-based strategy, i.e., applying filters to data segments excluding the artifact window, to minimize distortion from abrupt TMS-related transients. Overall, this work represents an important step toward establishing a general preprocessing framework for TMS-iEEG data. We hope it encourages broader adoption and methodological development in concurrent TMS-iEEG research, ultimately advancing our understanding of brain organization and TMS mechanisms. HighlightsO_LIWe presented a practical preprocessing pipeline for single pulse TMS-iEEG data, incorporating key steps of re-referencing, filtering, artifact interpolation, and detrending. C_LIO_LIThe pipeline effectively attenuates multiple types of artifacts and noise, enabling accurate characterization of evoked neural responses. C_LIO_LIMethodological alternatives for each preprocessing step were evaluated using real and/or simulated datasets. C_LIO_LIRe-referencing substantially affects the morphology and amplitude of intracranial TMS-evoked potentials and requires careful consideration. C_LIO_LIA segment-based filtering strategy is recommended to better minimize distortion from TMS-related artifacts. C_LI

neuroscience↗

Neuroanatomical Basis of Coma in Acute Ischemic Stroke

BackgroundAcute ischemic stroke (AIS) can lead to profound disturbances in consciousness, including coma, which is associated with poor prognosis and increased mortality. Clarifying the lesion patterns that precipitate loss of consciousness can refine pathophysiological models and guide prognosis. ObjectivesIn this study, we aim to identify the brain regions most commonly affected in comatose AIS and determine whether specific combinations of lesions are necessary and sufficient to produce coma. MethodsWe retrospectively analyzed 476 AIS patients (52 comatose) using diffusion-weighted imaging. Infarcts were automatically segmented, manually verified, and normalized to MNI space. Support vector regression lesion-symptom mapping (SVR-LSM) quantified voxel-wise associations with coma, controlling for lesion volume. To assess the necessity and sufficiency of lesion combinations, we employed permutation-based nested logistic regression models comparing all subsets of four anatomical predictors: brainstem, thalamus, cerebellum, and the rest of brain lesions. ResultsSVR-LSM revealed that coma was strongly associated with lesions involving the brainstem, thalamus, and cerebellum, whereas non-comatose patients exhibited predominantly cortical infarcts. Nested model comparisons showed that concurrent lesions to both the brainstem and thalamus were necessary and sufficient for coma. Additional involvement of the cerebellum or cerebral cortex did not improve predictive performance. ConclusionsComa after AIS results from a dual-node subcortical lesion pattern involving both the brainstem and thalamus. Cerebellar and cortical lesions, even when extensive, did not induce coma in the absence of the dual-brainstem and thalamic lesions. These observations emphasize the predominant role of lesion location over lesion volume in the pathogenesis of coma. They also support mechanistic models that position the brainstem and thalamic hubs as central to the neural circuitry underlying arousal. Furthermore, these findings delineate a specific anatomical substrate that may serve as a strategic target for circuit-based neuroprotective and neuromodulatory therapies.

neuroscience↗

Multimodal Evidence for Hippocampal Engagement and Modulation by Functional Connectivity-Guided Parietal TMS

Hippocampal activity supports memory and many other brain functions. Transcranial magnetic stimulation (TMS) guided by hippocampal functional connectivity (FC) shows promise in improving memory, but direct neural evidence of its capacity to engage and modulate hippocampal activity is lacking. Here we combined TMS with intracranial electroencephalography (iEEG) in 8 neurosurgical patients and with functional magnetic resonance imaging (fMRI) in 79 neurologically healthy participants. We identified that (1) single-pulse TMS to individualized parietal cortex guided by hippocampal-FC preferentially evoked distinct temporal and spectral activity patterns in the hippocampus, (2) variability in TMS-evoked hippocampal responses related to individual differences in parietal-hippocampus FC strength, and (3) repetitive TMS to hippocampal-FC-guided parietal cortex selectively suppressed hippocampal theta oscillations. These findings provide multimodal causal neural evidence and important mechanistic insights supporting the development of personalized neuromodulation strategies aimed at improving hippocampus-dependent functions.

neuroscience↗

DLPFC Stimulation Suppresses High-Frequency Neural Activity in the Human sgACC

Transcranial magnetic stimulation (TMS) to the dorsolateral prefrontal cortex (DLPFC) is hypothesized to relieve symptoms of depression by inhibiting activity in the subgenual anterior cingulate cortex (sgACC). However, we have a limited understanding of how TMS influences neural activity in the sgACC, owing to its deep location within the brain. To better understand the mechanism of antidepressant response to TMS, we recruited two neurosurgical patients with indwelling electrodes and delivered TMS pulses to the DLPFC while simultaneously recording local field potentials from the sgACC. Spectral analysis revealed a decrease in high-frequency activity (HFA; 70-180 Hz) after each stimulation pulse, which was especially pronounced in the sgACC relative to other regions. TMS-evoked HFA power was generally anticorrelated between the DLPFC and sgACC, even while low-frequency phase locking between the two regions was enhanced. Together, these findings support the notion that TMS to the DLPFC can suppress neural firing in the sgACC, suggesting a possible mechanism by which this treatment regulates mood.

neuroscience↗

Dorsolateral prefrontal cortex TMS evokes responses in the subgenual anterior cingulate cortex: Evidence from human intracranial EEG

Transcranial magnetic stimulation combined with intracranial local field potential recordings in humans (TMS-iEEG) represents a new method for investigating electrophysiologic effects of TMS with spatiotemporal precision. We applied TMS-iEEG to the dorsolateral prefrontal cortex (dlPFC) in two subjects and demonstrate evoked activity in the subgenual anterior cingulate cortex (sgACC). This study provides direct electrophysiologic evidence that dlPFC TMS, as targeted for depression treatment, can modulate brain activity in the sgACC.

neuroscience↗

Iowa Brain-Behavior Modeling Toolkit: An Open-Source MATLAB Tool for Inferential and Predictive Modeling of Imaging-Behavior and Lesion-Deficit Relationships

The traditional analytical framework taken by neuroimaging studies in general, and lesion-behavior studies in particular, has been inferential in nature and has focused on identifying and interpreting statistically significant effects within the sample under study. While this framework is well-suited for hypothesis testing approaches, achieving the modern goal of precision medicine requires a different framework that is predictive in nature and that focuses on maximizing the predictive power of models and evaluating their ability to generalize beyond the data that were used to train them. However, few tools exist to support the development and evaluation of predictive models in the context of neuroimaging or lesion-behavior research, creating an obstacle to the widespread adoption of predictive modeling approaches in the field. Further, existing tools for lesion-behavior analysis are often unable to accommodate categorical outcome variables and often impose restrictions on the predictor data. Researchers therefore often must use different software packages and analytical approaches depending on whether they are addressing a classification vs. regression problem and on whether their predictor data correspond to binary lesion images, continuous lesion-network images, connectivity matrices, or other data modalities. To address these limitations, we have developed a MATLAB software toolkit that supports both inferential and predictive modeling frameworks, accommodates both classification and regression problems, and does not impose restrictions on the modality of the predictor data. The toolkit features both a graphical user interface and scripting interface, includes implementations of multiple mass-univariate, multivariate, and machine learning models, features built-in and customizable routines for hyper-parameter optimization, cross-validation, model stacking, and significance testing, and automatically generates text-based descriptions of key methodological details and modeling results to improve reproducibility and minimize errors in the reporting of methods and results. Here, we provide an overview and discussion of the toolkits features and demonstrate its functionality by applying it to the question of how expressive and receptive language impairments relate to lesion location, structural disconnection, and functional network disruption in a large sample of patients with left hemispheric brain lesions. We find that impairments in expressive vs. receptive language are most strongly associated with left lateral prefrontal and left posterior temporal/parietal damage, respectively. We also find that impairments in expressive vs. receptive language are associated with partially overlapping patterns of fronto-temporal structural disconnection, and that the associated functional networks are also similar. Importantly, we find that lesion location and lesion-derived network measures are highly predictive of both types of impairment, with predictions from models trained on these measures explaining [~]30-40% of the variance on average when applied to data from patients not used to train the models. We have made the toolkit publicly available, and we have included a comprehensive set of tutorial notebooks to support new users in applying the toolkit in their studies. Key PointsO_LIWe describe a new MATLAB toolkit for inferential and predictive modeling of imaging datasets. C_LIO_LIWe demonstrate the application of the toolkit to real lesion, network, and behavioral datasets. C_LIO_LIWe have made the toolkit publicly available to the research community. C_LI

neuroscience↗

TMS provokes target-dependent intracranial rhythms across human cortical and subcortical sites

Transcranial magnetic stimulation (TMS) is increasingly deployed in the treatment of neuropsychiatric illness, under the presumption that stimulation of specific cortical targets can alter ongoing neural activity and cause circuit-level changes in brain function. While the electrophysiological effects of TMS have been extensively studied with scalp electroencephalography (EEG), this approach is most useful for evaluating low-frequency neural activity at the cortical surface. As such, little is known about how TMS perturbs rhythmic activity among deeper structures - such as the hippocampus and amygdala - and whether stimulation can alter higher-frequency oscillations. Recent work has established that TMS can be safely used in patients with intracranial electrodes (iEEG), allowing for direct neural recordings at sufficient spatiotemporal resolution to examine localized oscillatory responses across the frequency spectrum. To that end, we recruited 17 neurosurgical patients with indwelling electrodes and recorded neural activity while patients underwent repeated trials of single-pulse TMS at several cortical sites. Stimulation to the dorsolateral prefrontal cortex (DLPFC) drove widespread low-frequency increases (3-8Hz) in frontolimbic cortices, as well as high-frequency decreases (30-110Hz) in frontotemporal areas, including the hippocampus. Stimulation to parietal cortex specifically provoked low-frequency responses in the medial temporal lobe. While most low-frequency activity was consistent with brief evoked responses, anterior frontal regions exhibited induced theta oscillations following DLPFC stimulation. Taken together, we established that non-invasive stimulation can (1) provoke a mixture of low-frequency evoked power and induced theta oscillations and (2) suppress high-frequency activity in deeper brain structures not directly accessed by stimulation itself.

neuroscience↗

Data-driven biomarkers outperform theory-based biomarkers in predicting stroke motor outcomes

Chronic motor impairments are a leading cause of disability after stroke. Previous studies have predicted motor outcomes based on the degree of damage to predefined structures in the motor system, such as the corticospinal tract. However, such theory-based approaches may not take full advantage of the information contained in clinical imaging data. The present study uses data-driven approaches to predict chronic motor outcomes after stroke and compares the accuracy of these predictions to previously-identified theory-based biomarkers. Using a cross-validation framework, regression models were trained using lesion masks and motor outcomes data from 789 stroke patients (293 female/496 male) from the ENIGMA Stroke Recovery Working Group (age 64.9{+/-}18.0 years; time since stroke 12.2{+/-}0.2 months; normalised motor score 0.7{+/-}0.5 (range [0,1]). The out-of-sample prediction accuracy of two theory-based biomarkers was assessed: lesion load of the corticospinal tract, and lesion load of multiple descending motor tracts. These theory-based prediction accuracies were compared to the prediction accuracy from three data-driven biomarkers: lesion load of lesion-behaviour maps, lesion load of structural networks associated with lesion-behaviour maps, and measures of regional structural disconnection. In general, data-driven biomarkers had better prediction accuracy - as measured by higher explained variance in chronic motor outcomes - than theory-based biomarkers. Data-driven models of regional structural disconnection performed the best of all models tested (R2 = 0.210, p < 0.001), performing significantly better than predictions using the theory-based biomarkers of lesion load of the corticospinal tract (R2 = 0.132, p< 0.001) and of multiple descending motor tracts (R2 = 0.180, p < 0.001). They also performed slightly, but significantly, better than other data-driven biomarkers including lesion load of lesion-behaviour maps (R2 =0.200, p < 0.001) and lesion load of structural networks associated with lesion-behaviour maps (R2 =0.167, p < 0.001). Ensemble models - combining basic demographic variables like age, sex, and time since stroke - improved prediction accuracy for theory-based and data-driven biomarkers. Finally, combining both theory-based and data-driven biomarkers with demographic variables improved predictions, and the best ensemble model achieved R2 = 0.241, p < 0.001. Overall, these results demonstrate that models that predict chronic motor outcomes using data-driven features, particularly when lesion data is represented in terms of structural disconnection, perform better than models that predict chronic motor outcomes using theory-based features from the motor system. However, combining both theory-based and data-driven models provides the best predictions.

neuroscience↗

Improved high-dimensional multivariate autoregressive model estimation of human electrophysiological data using fMRI priors

Multivariate autoregressive (MVAR) model estimation enables assessment of causal interactions in brain networks. However, accurately estimating MVAR models for high-dimensional electrophysiological recordings is challenging due to the extensive data requirements. Hence, the applicability of MVAR models for study of brain behavior over hundreds of recording sites has been very limited. Prior work has focused on different strategies for selecting a subset of important MVAR coefficients in the model and is motivated by the potential of MVAR models and the data requirements of conventional least-squares estimation algorithms. Here we propose incorporating prior information, such as fMRI, into MVAR model estimation using a weighted group LASSO regularization strategy. The proposed approach is shown to reduce data requirements by a factor of two relative to the recently proposed group LASSO method of Endemann et al. (2022) while resulting in models that are both more parsimonious and have higher fidelity to the ground truth. The effectiveness of the method is demonstrated using simulation studies of physiologically realistic MVAR models derived from iEEG data. The robustness of the approach to deviations between the conditions under which the prior information and iEEG data is obtained is illustrated using models from data collected in different sleep stages. This approach will allow accurate effective connectivity analyses over short time scales, facilitating investigations of causal interactions in the brain underlying perception and cognition during rapid transitions in behavioral state.

neuroscience↗

Lesion Localization of Time Disorientation in Patients With Focal Brain Damage

Background and ObjectivesTime orientation is a fundamental cognitive process in which ones personal sense of time is matched with a universal reference. Assessment of time orientation is a ubiquitous component of neurological mental status examinations and neuropsychological assessments, yet its neural correlates remain unclear. Large bilateral lesions have been associated with deficits in time orientation, but more specific regions of the brain implicated in time disorientation following focal unilateral damage are relatively unknown. The current study investigates the anatomy of time disorientation and its network correlates in patients with focal brain lesions. Methods550 patients with acquired, focal brain lesions participated in this study, identified retrospectively from the Iowa Neurological Patient Registry. Time orientation was assessed 3 months or more after lesion onset using the Benton Temporal Orientation Test (BTOT), and 39 patients were identified as having chronic impairment in time orientation defined as a score of 3 or worse on the BTOT. Multivariate lesion-symptom mapping and lesion network mapping were used to evaluate the anatomy and networks associated with time disorientation. Performance on a variety of neuropsychological tests was compared between the time oriented and time disoriented group. Results39 patients were identified as having chronic impairment in time orientation. Multivariate lesion-symptom mapping showed that lesions of the posterior cortices were associated with impaired time orientation, including medial temporal lobes, occipitotemporal cortex, and precuneus (r=0.21, p<.001). Individuals with time disorientation tended to have concomitant impairments in memory, visuospatial ability, and naming. Follow-up analyses of individuals with unilateral lesions and those with relatively unimpaired cognition in other domains implicated the precuneus and parahippocampal gyrus in time orientation. Lesion network mapping demonstrated that these regional findings occurred at nodes of the default mode and visual networks. Individuals with time disorientation tended to have concomitant impairments in memory, visuospatial ability, and naming. DiscussionWe interpret these findings as novel evidence for the role of posteromedial cortices extending from the precuneus to the medial temporal lobe in supporting time orientation.

neuroscience↗

Functional geometry of auditory cortical resting state networks derived from intracranial electrophysiology

Understanding central auditory processing critically depends on defining underlying auditory cortical networks and their relationship to the rest of the brain. We addressed these questions using resting state functional connectivity derived from human intracranial electroencephalography. Mapping recording sites into a low-dimensional space where proximity represents functional similarity revealed a hierarchical organization. At fine scale, a group of auditory cortical regions excluded several higher order auditory areas and segregated maximally from prefrontal cortex. On mesoscale, the proximity of limbic structures to auditory cortex suggested a limbic stream that parallels the classically described ventral and dorsal auditory processing streams. Identities of global hubs in anterior temporal and cingulate cortex depended on frequency band, consistent with diverse roles in semantic and cognitive processing. On a macro scale, observed hemispheric asymmetries were not specific for speech and language networks. This approach can be applied to multivariate brain data with respect to development, behavior, and disorders. BlurbWe describe the organization of human neocortex on multiple spatial scalesbased on resting state intracranial electrophysiology. We focus on cortical regions involved in auditory processing and examine inter-regional hierarchical relationships, network topology, and hemispheric lateralization. This work introduces a powerful analytical tool to examine mechanisms of altered arousal states, brain development, and neuropsychiatric disorders.

neuroscience↗