Biology subjects

Verhagen, L.

Publications and source records attributed to Verhagen, L..

At least 19 recordsLinked to original sources

bioRxiv2026

Transcranial ultrasound stimulation of the aMCC transiently improves performance, modulates N2 and conflict monitoring dynamics

Conflict monitoring and error processing are fundamental mechanisms underlying cognitive control and adaptive behavior and have been consistently associated with increased activity in the anterior midcingulate cortex (aMCC). Here, we used transcranial ultrasound stimulation (TUS), an emerging technique that enables non-invasive, deep, and focal neuromodulation, and EEG to investigate the causal role of the aMCC in cognitive control. Our findings demonstrate that TUS of aMCC improved performance, modulated the relationship between conflict monitoring and the stimulus-locked N2, and strengthened the suppression of distracting flankers as revealed by drift-diffusion model analyses. This suggests that TUS of aMCC enhances proactive control. Interestingly, TUS did not affect the error-related negativity as a measure of error monitoring. Finally, the TUS effects were observed during early compared with later task blocks corroborating previous findings which suggested that TUS effects are temporally dynamic and characterized by a limited post-stimulation window. HIGHLIGHTSO_LIaMCC-TUS and PCC-TUS both increase behavioral accuracy during the early stages of task performance. C_LIO_LIaMCC-TUS transiently reduces the effect of incongruence on the stimulus-locked N2 suggesting reduced response conflict. C_LIO_LIExploratory DDM analyses suggest that aMCC-TUS improves suppression of conflict- inducing distractors. C_LIO_LIaMCC thus selectively enhances proactive control, thereby reducing response conflict. C_LIO_LITUS effects show a transient temporal profile, peaking 17-27 minutes after stimulation and declining after [~]37 minutes. C_LI

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bioRxiv2025

Parameter optimisation for mitigating somatosensory confounds during transcranial ultrasonic stimulation

Transcranial ultrasonic stimulation (TUS) redefines what is possible with non-invasive neuromodulation by oaering unparalleled spatial precision and flexible targeting capabilities. However, peripheral confounds pose a significant challenge to reliably implementing this technology. While auditory confounds during TUS have been studied extensively, the somatosensory confound has been overlooked thus far. It will become increasingly vital to quantify and manage this confound as the field shifts towards higher doses, more compact stimulation devices, and more frequent stimulation through the temple where co-stimulation is more pronounced. Here, we provide a systematic characterisation of somatosensory co-stimulation during TUS. We also identify the conditions under which this confound can be mitigated most eaectively by mapping the confound-parameter space. Specifically, we investigate dose-response eaects, pulse shaping characteristics, and transducer-specific parameters. We demonstrate that somatosensory confounds can be mitigated by avoiding near-field intensity peaks in the scalp, spreading energy across a greater area of the scalp, ramping the pulse envelope, and delivering equivalent doses via longer, lower-intensity pulses rather than shorter, higher-intensity pulses. Additionally, higher pulse repetition frequencies and fundamental frequencies reduce somatosensory eaects. Through our systematic mapping of the parameter space, we also find preliminary evidence that particle displacement (strain) may be a primary biophysical driving force behind peripheral somatosensory co-stimulation. This study provides actionable strategies to minimise somatosensory confounds, which will support the thorough experimental control required to unlock the full potential of TUS for scientific research and clinical interventions. Highlights- Tactile, thermal, and even painful somatosensory confounds may occur during TUS. - Confounds can be mitigated via pulse shaping & transducer-specific parameters. - Valid and replicable TUS research requires control for peripheral confounds. - Particle displacement may be a primary driving force for somatosensory confounds.

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bioRxiv2025

Rapid modulation of choice behavior by ultrasound on the human frontal eye fields

A fundamental challenge in neuroscience is establishing causal brain-function relationships with spatial and temporal precision. Transcranial ultrasonic stimulation (TUS) offers a unique opportunity to modulate deep brain structures non-invasively with high spatial resolution, but temporally precise effects and their neurophysiological foundations have yet to be demonstrated in humans. Here, we develop a temporally precise TUS protocol targeting the frontal eye fields (FEFs) -- a well-characterized circuit critical for saccadic eye movements. We demonstrate that TUS induces robust excitatory behavioral effects. Importantly, individual differences in baseline GABAergic inhibitory tone predict response magnitude. These findings establish TUS as a reliable tool for chronometric circuit interrogation and highlight the importance of neurophysiological state in neuromodulation. This work bridges human and animal research, advancing targeted TUS applications in neuroscience and clinical settings. HighlightsO_LIFocused ultrasound modulates saccades with high spatial and temporal precision C_LIO_LIInhibitory circuits in the frontal eye fields shape choice computations C_LIO_LIGABA levels predict individual variability in ultrasound-induced behavioral changes C_LIO_LIUltrasound can be used to probe fast neural dynamics and individual differences C_LI

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bioRxiv2024

Failed Double-Blind Replication of Offline 5Hz-rTUS-Induced Corticospinal Excitability

IntroductionTranscranial ultrasound stimulation (TUS) is a promising new form of non-invasive neuromodulation. As a nascent technique, replication of its effects on brain function is important. Of particular interest is offline 5Hz repetitive TUS (5Hz-rTUS), originally reported by Zeng and colleagues [1] to elicit lasting corticospinal excitability increases, with large effect sizes. Material and methodHere, we conducted a pre-registered (https://osf.io/p5n4q) replication of this protocol that benefitted from three additional features: double-blind application of TUS, neuronavigation for consistent TMS positioning, and acoustic simulations to assess M1 target exposure to TUS. Changes in resting motor thresholds (rMT), motor-evoked potential (MEP) amplitude, short-interval intracortical inhibition (SICI) and intracortical facilitation (ICF) in response to TUS (5Hz-rTUS vs. sham) were measured in the right first dorsal interosseous (FDI), abductor digiti minimi (ADM) and abductor pollicis brevis (APB) muscles, with unbiased selection of participants. Transducer location was determined by the TMS-hotspot for motor representations of the right FDI, as in the original work. ResultsNo significant effects of 5Hz-TUS (vs sham) were observed. Post-hoc simulations showed considerable variability of the acoustic focus, which was outside the anatomical M1-hand area in 67% of participants - in line with the known poor correspondence of TMS-hotspot location and M1-hand area. ConclusionOur results indicate that the effect sizes of the neuromodulatory effects of 5Hz-rTUS on M1 may be more variable than previously appreciated. We suggest that double-blinding, neuronavigated TMS, individualised acoustic simulations for TUS targeting and pre-registration will aid reproducibility across studies.

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bioRxiv2023

Auditory confounds can drive online effects of transcranial ultrasonic stimulation in humans

Transcranial ultrasonic stimulation (TUS) is rapidly emerging as a promising non-invasive neuromodulation technique. TUS is already well-established in animal models, providing foundations to now optimize neuromodulatory efficacy for human applications. Across multiple studies, one promising protocol, pulsed at 1000 Hz, has consistently resulted in motor cortical inhibition in humans (Fomenko et al., 2020). At the same time, a parallel research line has highlighted the potentially confounding influence of peripheral auditory stimulation arising from TUS pulsing at audible frequencies. In this study, we disentangle direct neuromodulatory and indirect auditory contributions to motor inhibitory effects of TUS. To this end, we include tightly matched control conditions across four experiments, one preregistered, conducted independently at three institutions. We employed a combined transcranial ultrasonic and magnetic stimulation paradigm, where TMS-elicited motor-evoked potentials (MEPs) served as an index of corticospinal excitability. First, we replicated motor inhibitory effects of TUS but showed through both tight controls and manipulation of stimulation intensity, duration, and auditory masking conditions that this inhibition was driven by peripheral auditory stimulation, not direct neuromodulation. Further, we consider neuromodulation beyond driving overall excitation/inhibition and show preliminary evidence of how TUS might interact with ongoing neural dynamics instead. Primarily, this study highlights the substantial shortcomings in accounting for the auditory confound in prior TUS-TMS work where only a flip-over sham and no active control was used. The field must critically reevaluate previous findings given the demonstrated impact of peripheral confounds. Further, rigorous experimental design via (in)active control conditions is required to make substantiated claims in future TUS studies. Only when direct effects are disentangled from those driven by peripheral confounds can TUS fully realize its potential for research and clinical applications.

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bioRxiv2023

Transcranial focused ultrasound-mediated neurochemical and functional connectivity changes in deep cortical regions in humans

Low-intensity transcranial ultrasound stimulation (TUS) is an emerging non-invasive technique for focally modulating human brain function. The mechanisms and neurochemical substrates underlying TUS neuromodulation in humans and how these relate to excitation and inhibition are still poorly understood. In 24 healthy controls, we separately stimulated two deep cortical regions and investigated the effects of theta-burst TUS, a protocol shown to increase corticospinal excitability, on the inhibitory neurotransmitter gamma-aminobutyric acid (GABA) and functional connectivity. We show for the first time in humans that theta-burst TUS selectively reduces GABA levels in the posterior cingulate, but not the dorsal anterior cingulate cortex. Functional connectivity increased following TUS in both regions. Our findings suggest that TUS changes overall excitability by reducing GABAergic inhibition, that changes in TUS-mediated neuroplasticity last at least 50 minutes after stimulation, and that these effects may be state-dependent - a mechanism increasingly recognized to influence the brains response to neuromodulation.

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bioRxiv2021

Social prediction modulates activity of macaque superior temporal cortex

The ability to attribute thoughts to others, also called theory of mind (TOM), has been extensively studied. Computationally, the basis of TOM in humans has been interpreted within the predictive coding framework and associated with activity in the temporo-parietal junction (TPJ). However, the evolutionary origins of these human mindreading abilities have been challenged since the concept was coined. Here we identify a brain region in the Rhesus macaque that shares computational properties with the human TPJ. We revealed, using a non-linguistic task and functional magnetic resonance imaging, that activity in a region of the macaque middle superior temporal cortex was specifically modulated by the predictability of social interactions. As in human TPJ, this region could be distinguished from other temporal regions involved in face processing. Our result suggests the existence of a precursor for the theory of mind ability in the last common ancestor of human and old-world monkeys.

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bioRxiv2020

Heterogeneous relationships between white matter and behaviour

Several studies have established specific relationships between White Matter (WM) and behaviour. However, these studies have typically focussed on fractional anisotropy (FA), a neuroimaging metric that is sensitive to multiple tissue properties, making it difficult to identify what biological aspects of WM may drive such relationships. Here, we carry out a pre-registered assessment of WM-behaviour relationships in 50 healthy individuals across multiple behavioural and anatomical domains, and complementing FA with myelin-sensitive quantitative MR modalities (MT, R1, R2*). Surprisingly, we only find support for predicted relationships between FA and behaviour in one of three pre-registered tests. For one behavioural domain, where we failed to detect an FA-behaviour correlation, we instead find evidence for a correlation between behaviour and R1. This hints that multimodal approaches are able to identify a wider range of WM-behaviour relationships than focusing on FA alone. To test whether a common biological substrate such as myelin underlies WM-behaviour relationships, we then ran joint multimodal analyses, combining across all MRI parameters considered. No significant multimodal signatures were found and power analyses suggested that sample sizes of 40 to 200 may be required to detect such joint multimodal effects, depending on the task being considered. These results demonstrate that FA-behaviour relationships from the literature can be replicated, but may not be easily generalisable across domains. Instead, multimodal microstructural imaging may be best placed to detect a wider range of WM-behaviour relationships, as different MRI modalities provide distinct biological sensitivities. Our findings highlight a broad heterogeneity in WMs relationship with behaviour, suggesting that variable biological effects may be shaping their interaction. HighlightsO_LIPre-registered testing of microstructural imaging across modalities (FA, MT, R1, R2*) to test WM-behaviour relationships. C_LIO_LIPartial support for FA-behaviour relationships hypothesised based on previous literature. C_LIO_LIMultimodal approaches can help detect WM-behaviour relationships that are not detected with FA alone. C_LIO_LISample sizes of 40 to 200 may be needed to detect myelin-behaviour relationships in joint multimodal analyses. C_LIO_LIVariable biological effects may be shaping WM-behaviour relationships. C_LI

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bioRxiv2020

Entraining corticocortical plasticity changes oscillatory activity in action control and inhibition

Oscillatory activity may reflect interactions between brain areas[1]. Here we tested whether inducing corticocortical plasticity in a specific set of connections changes oscillatory activity and cortico-cortical interactions and, if this is the case, whether the changes manifest in a manner that is behaviour state-dependent. We either increased or decreased the influence of activity in human ventral premotor cortex (PMv) over activity in primary motor cortex (M1) using cortico-cortical paired associative stimulation (ccPAS)[2, 3]. Before and after stimulation participants performed a Go/No-Go task. While M1 TMS pulses revealed the excitatory state of the motor system at specific time points, the electroencephalogram (EEG) revealed the evolution of oscillatory activity dynamics in the motor system over several hundreds of milliseconds before, during, and after each movement. Augmenting cortical connectivity between PMv and M1, by evoking synchronous pre- and postsynaptic activity in the PMv-M1 pathways, led to a state-dependent modulation of the causal influence of PMv over M1, and at the same time, enhanced oscillatory beta and theta rhythms in Go and No-Go trials, respectively. No changes were observed in the alpha rhythm. The plasticity induction effect was dependent on PMv-M1 stimulation order; the opposite patterns of results were observed after an equal amount of stimulation of PMv and M1 but applied in a temporal pattern that did not augment PMvs influence over M1. These results are consistent with Hebbian principles of synaptic plasticity[4] and show that artificial manipulation of cortico-cortical connectivity produces state-dependent functional changes in the spectral fingerprints of the motor circuit.

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bioRxiv2020

Anatomically precise relationship between specific amygdala connections and selective markers of mental well-being in humans

There has been increasing interest in using neuroimaging measures to predict psychiatric disorders. However, predictions usually rely on large numbers of brain connections and large disorder heterogeneity, thus lacking both anatomical and behavioural specificity, preventing the advancement of targeted interventions. Here, we address both challenges. First, using resting-state functional MRI, we parcellated the amygdala, a region implicated in mood disorders but difficult to image with high fidelity, into seven nuclei. Next, a questionnaire factor analysis provided four sub-clinical latent behaviours frequently found in anxious-depressive individuals, such as negative emotions and sleep problems. Finally, for each latent behaviour, we identified the most predictive connections between individual amygdala nuclei and highly specific regions of interest e.g. dorsal raphe nucleus in the brainstem or medial prefrontal cortical regions. A small number of distinct connections predicted behaviours, providing unprecedented levels of specificity, in humans, for relating mental well-being to precise anatomical connections.

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bioRxiv2020

Double-dissociation of frequency-specific contributions of dorso-lateral and dorso-medial prefrontal cortex to familiarity and recollective processes in the primate

According to dual-process theories, recognition memory draws upon both familiarity and recollection. It remains unclear how primate prefrontal cortex (PFC) contributes to familiarity and recollection processes but frequency-specific neuronal activities are considered to play a key role. Here, non-human primate (NHP) electrophysiological local field potential (LFP) recordings first showed that a specific subregion of macaque PFC (i.e., dorsolateral PFC, dlPFC) was implicated in task performance at a specific frequency (i.e., increased beta power in the 10-15 Hz range observed in correct versus error trials) in a specific phase of a recognition memory task (i.e., during sample presentation). Then, to assess generalization to humans and causality we targeted left human dlPFC (BA 9/46) as well as left dorsomedial prefrontal cortex (BA 8/9) for comparison, and also vertex as a control, with transcranial magnetic stimulation at a frequency in the middle of the low-beta range observed in NHP (i.e. 12.5 Hz) and compared that to non-frequency-specific stimulation, and also to a no-stimulation control, during occasional sample presentations within a similar task. Hence we investigated hypotheses about the causal importance for human memory of a location-specific, frequency-specific, and task-epoch-specific intervention derived directly from the NHP electrophysiological observations. Using a dual-process signal detection (DPSD) model based on analysing receiver operating characteristics (ROC) curves, we showed beta-frequency TMS caused decreased recollection when targeted to human dlPFC, but enhanced familiarity when targeted to dorsomedial prefrontal cortex. Non-frequency-specific patterns of stimulation to all sites, and beta-frequency stimulation to vertex, were all without behavioural effect. This study provides causal evidence that PFC-mediated contributions to object recognition memory are modulated by beta-frequency activity; more broadly it provides translational evidence bridging NHPs and humans by emphasizing functional roles of beta-frequency activity in homologous brain regions in recognition memory. HighlightsO_LIlow beta power in NHP dlPFC during stimulus encoding was related to behaviour C_LIO_LIhuman rTMS study used parameters derived from NHP observations to test causality C_LIO_LIlow beta rTMS to human dlPFC, but not dmPFC, impairs recollection C_LIO_LIlow beta rTMS to human dmPFC, but not dlPFC, enhances familiarity C_LIO_LIprovides cross-species validation of prefrontal beta power to primate recognition C_LI

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bioRxiv2019

Human lateral Frontal Pole contributes to control over social-emotional behaviour

Regulation of emotional behavior is essential for human social interactions. Recent work has exposed its cognitive complexity, as well as its unexpected reliance on portions of the anterior prefrontal cortex (aPFC) also involved in exploration, relational reasoning, and counterfactual choice, rather than on dorsolateral and medial prefrontal areas involved in several forms of cognitive control. This study anatomically qualifies the contribution of aPFC territories to the regulation of social-emotional actions, and explores a possible structural pathway through which emotional regulation might be implemented. We provide converging evidence from task-based fMRI, diffusion-weighted imaging, and functional connectivity fingerprints for a novel neural element in emotional regulation. Task-based fMRI in human male participants (N = 40) performing a social-emotional approach-avoidance task identified aPFC territories involved in the regulation of social-emotional actions. Connectivity fingerprints, based on diffusion-weighted imaging and resting-state connectivity, localized those task-defined frontal regions to the lateral frontal pole (FPl), an anatomically-defined portion of the aPFC that lacks a homologous counterpart in macaque brains. Probabilistic tractography indicated that 10-20% of inter-individual variation in social-emotional regulation abilities is accounted for by the strength of structural connectivity between FPl and amygdala. Evidence from an independent replication sample (N = 50; 10 females) further substantiated this result. These findings provide novel neuroanatomical evidence for incorporating FPl in models of control over human social-emotional behavior. Significance statementSuccessful regulation of emotional behaviors is a prerequisite for successful participation in human society, as is evidenced by the social isolation and loss of occupational opportunities often encountered by people suffering from emotion-regulation disorders such as social-anxiety disorder and psychopathy. Knowledge about the precise cortical regions and connections supporting this control is crucial for understanding both the nature of computations needed to successfully traverse the space of possible actions in social situations, and the potential interventions that might result in efficient treatment of social-emotional disorders. This study provides evidence for a precise cortical region (FPl) and a structural pathway (the ventral amygdalofugal bundle) through which a cognitively complex form of emotional action regulation might be implemented in the human brain.

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bioRxiv2019

Two fiber pathways connecting amygdala and prefrontal cortex in humans and monkeys

The interactions between amygdala and prefrontal cortex are pivotal to many neural processes involved in learning, decision-making, emotion, and social regulation. The broad functional role of amygdala-prefrontal interplay may reflect the diversity of its anatomical connections. Little, however, is known of the structural wiring linking amygdala and prefrontal cortex in humans. Using diffusion imaging techniques, we reconstructed connections between amygdala, anterior temporal and prefrontal cortex in human and macaque brains. First, by studying macaques we were able to assess which aspects of connectivity known from tracer studies could be identified with diffusion imaging. Second, by comparing diffusion imaging results in humans and macaques we were able to estimate amygdala-prefrontal connection patterns in humans and compare them with those in the monkey. We observed a prominent and well-preserved bifurcation of connections between amygdala and frontal lobe into two fiber networks - an amygdalofugal path and an uncinate fascicle path - in both species.

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bioRxiv2018

The human ventromedial prefrontal cortex sulcal morphology and its influence on its functional organization.

The ventromedial prefrontal cortex (vmPFC), which comprises several distinct cytoarchitectonic areas, is a key brain region supporting decision-making processes and it has been shown to be one of the main hubs of the Default Mode Network, a network classically activated during resting state. We here examined the inter-individual variability in the vmPFC sulcal morphology in 57 humans (37 females) and demonstrated that the presence/absence of the inferior rostral sulcus and the subgenual intralimbic sulcus influences significantly the sulcal organization of this region. Furthermore, the sulcal organization influences the location of the vmPFC peak of the Default Mode Network, demonstrating that the location of functional activity can be affected by local sulcal patterns. These results are critical for the investigation of the function of the vmPFC and show that taking into account the sulcal variability might be essential to guide the interpretation of neuroimaging studies.\n\nSIGNIFICANCE STATEMENTThe ventromedial prefrontal cortex (vmPFC) is one of the main hubs of the Default Mode Network and plays a central role in value coding and decision-making. The present study provides a complete description of the inter-individual variability of anatomical morphology of this large portion of prefrontal cortex and its relation to functional organization. We have shown that two supplementary medial sulci predominantly determine the organization of the vmPFC, which in turn affect the location of the functional peak of activity in this region. Those results show that taking into account the variability in sulcal patterns might be essential to guide the interpretation of neuroimaging studies of the human brain and of the vmPFC in particular.

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bioRxiv2018

The macaque anterior cingulate cortex translates counterfactual choice value into actual behavioral change

The neural mechanisms mediating sensory-guided decision making have received considerable attention but animals often pursue behaviors for which there is currently no sensory evidence. Such behaviors are guided by internal representations of choice values that have to be maintained even when these choices are unavailable. We investigated how four macaque monkeys maintained representations of the value of counterfactual choices - choices that could not be taken at the current moment but which could be taken in the future. Using functional magnetic resonance imaging, we found two different patterns of activity co-varying with values of counterfactual choices in a circuit spanning hippocampus, anterior lateral prefrontal cortex, and anterior cingulate cortex (ACC). ACC activity also reflected whether the internal value representations would be translated into actual behavioral change. To establish the causal importance of ACC for this translation process, we used a novel technique, Transcranial Focused Ultrasound Stimulation, to reversibly disrupt ACC activity.

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bioRxiv2018

Manipulation of deep brain activity in primates using transcranial focused ultrasound stimulation

The causal role of an area within a neural network can be determined by interfering with its activity and measuring the impact. Many current reversible manipulation techniques have limitations preventing their focal application particularly in deep areas of the primate brain. Here we demonstrate a transcranial focused ultrasound stimulation (TUS) protocol that manipulates activity even in deep brain areas: a subcortical brain structure, the amygdala (experiment 1), and a deep cortical region, anterior cingulate cortex (ACC, experiment 2), in macaques. TUS neuromodulatory effects were measured by examining relationships between activity in each area and the rest of the brain using functional magnetic resonance imaging (fMRI). In control conditions without sonication, activity in a given area is related to activity in interconnected regions but such relationships are reduced after sonication. Dissociable and focal effects on neural activity could not be explained by auditory artefacts.

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bioRxiv2018

Offline impact of transcranial focused ultrasound on cortical activation in primates

To understand brain circuits it is necessary both to record and manipulate their activity. Despite increased availability of techniques for manipulating neural activity in rodents, manipulating neural activity in primates remains difficult. Here we show that a minimally invasive technique, transcranial focused ultrasound stimulation (TUS), induced offline changes to activity of circumscribed brain regions in the macaque. Applying TUS to the supplementary motor area or frontal polar cortex resulted in spatially specific patterns of activity change measurable with functional magnetic resonance imaging. In each case changes reflected each areas known network of interactions with the rest of the brain. Independent of these specific neural effects, TUS over these regions also induced widespread signal changes that might have a non-neuronal origin possibly mediated by the cerebral spinal fluid compartment. Although sustained for more than one hour beyond the 40s stimulation period, TUS effects were reversible and not associated with histological changes.\n\nHighlights O_LIMany studies of ultrasound neuromodulation focus on online effects in rodents.\nC_LIO_LIWe use fMRI connectivity to investigate its offline impact in the primate brain.\nC_LIO_LI40 s of ultrasound leads to a sustained, specific, reversible neural modulation.\nC_LIO_LIUltrasound caused a sharpening of the stimulated regions connectivity profile.\nC_LI\n\nIn BriefA new application of focused ultrasound safely modulates brain activation in primates for up to 2 hours after 40 seconds of stimulation. Ultrasound caused the stimulated area to interact more selectively with the rest of the brain.

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bioRxiv2018

Whole brain comparative anatomy using connectivity blueprints

Comparing the brains of related species faces the challenges of establishing homologies whilst accommodating evolutionary specializations. Here we propose a general framework for understanding similarities and differences between the brains of primates. The approach uses white matter blueprints of the whole cortex based on a set of white matter tracts that can be anatomically matched across species. The blueprints provide a common reference space that allows us to navigate between brains of different species, identify homologue cortical areas, or to transform whole cortical maps from one species to the other. Specializations are cast within this framework as deviations between the species blueprints. We illustrate how this approach can be used to compare human and macaque brains.

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