EyeLink Non-Human Primate Publications
All EyeLink non-human primate research publications up until 2023 (with some early 2024s) are listed below by year. You can search the publications using keywords such as Temporal Cortex, Macaque, Antisaccade, etc. You can also search for individual author names. If we missed any EyeLink non-human primate articles, please email us!
2023 |
Michele Bevilacqua; Krystel R. Huxlin; Friedhelm C. Hummel; Estelle Raffin Pathway and directional specificity of Hebbian plasticity in the cortical visual motion processing network Journal Article In: iScience, vol. 26, no. 7, pp. 1–18, 2023. @article{Bevilacqua2023, Cortico-cortical paired associative stimulation (ccPAS), which repeatedly pairs single-pulse transcranial magnetic stimulation (TMS) over two distant brain regions, is thought to modulate synaptic plasticity. We explored its spatial selectivity (pathway and direction specificity) and its nature (oscillatory signature and perceptual consequences) when applied along the ascending (Forward) and descending (Backward) motion discrimination pathway. We found unspecific connectivity increases in bottom-up inputs in the low gamma band, probably reflecting visual task exposure. A clear distinction in information transfer occurred in the re-entrant alpha signals, which were only modulated by Backward-ccPAS, and predictive of visual improvements in healthy participants. These results suggest a causal involvement of the re-entrant MT-to-V1 low-frequency inputs in motion discrimination and integration in healthy participants. Modulating re-entrant input activity could provide single-subject prediction scenarios for visual recovery. Visual recovery might indeed partly rely on these residual inputs projecting to spared V1 neurons. |
Antonio Fernándeza; Nina M. Hanning; Marisa Carrasco Transcranial magnetic stimulation to frontal but not occipital cortex disrupts endogenous attention Journal Article In: Proceedings of the National Academy of Sciences, vol. 120, no. 10, pp. 1–10, 2023. @article{Fernandeza2023, Covert endogenous (voluntary) attention improves visual performance. Human neuroimaging studies suggest that the putative human homolog of macaque frontal eye fields (FEF+) is critical for this improvement, whereas early visual areas are not. Yet, correlational MRI methods do not manipulate brain function. We investigated whether rFEF+ or V1/V2 plays a causal role in endogenous attention. We used tran- scranial magnetic stimulation (TMS) to alter activity in the visual cortex or rFEF+ when observers performed an orientation discrimination task while attention was manipulated. On every trial, they received double-pulse TMS at a predetermined site (stimulated region) around V1/V2 or rFEF+. Two cortically magnified gratings were presented, one in the stimulated region (contralateral to the stimulated area) and another in the symmetric (ipsilateral) nonstimulated region. Grating contrast was varied to measure contrast response functions (CRFs) for all attention and stim- ulation combinations. In experiment 1, the CRFs were similar at the stimulated and nonstimulated regions, indicating that early visual areas do not modulate endogenous attention during stimulus presentation. In contrast, occipital TMS eliminates exog- enous (involuntary) attention effects on performance [A. Fernández, M. Carrasco,- Curr. Biol. 30, 4078–4084 (2020)]. In experiment 2, rFEF+ stimulation decreased the overall attentional effect; neither benefits at the attended location nor costs at the unattended location were significant. The frequency and directionality of microsaccades mimicked this pattern: Whereas occipital stimulation did not affect microsaccades, rFEF+ stimulation caused a higher microsaccade rate directed toward the stimulated hemifield. These results provide causal evidence of the role of this frontal region for endogenous attention. |
Nina M. Hanning; Antonio Fernández; Marisa Carrasco Dissociable roles of human frontal eye fields and early visual cortex in presaccadic attention Journal Article In: Nature Communications, vol. 14, no. 1, pp. 1–11, 2023. @article{Hanning2023, Shortly before saccadic eye movements, visual sensitivity at the saccade target is enhanced, at the expense of sensitivity elsewhere. Some behavioral and neural correlates of this presaccadic shift of attention resemble those of covert attention, deployed during fixation. Microstimulation in non-human primates has shown that presaccadic attention modulates perception via feedback from oculomotor to visual areas. This mechanism also seems plausible in humans, as both oculomotor and visual areas are active during saccade planning. We investigated this hypothesis by applying TMS to frontal or visual areas during saccade preparation. By simultaneously measuring perceptual performance, we show their causal and differential roles in contralateral presaccadic attention effects: Whereas rFEF+ stimulation enhanced sensitivity opposite the saccade target throughout saccade preparation, V1/V2 stimulation reduced sensitivity at the saccade target only shortly before saccade onset. These findings are consistent with presaccadic attention modulating perception through cortico-cortical feedback and further dissociate presaccadic and covert attention. |
2022 |
Marij Middag-van Spanje; Felix Duecker; Stefano Gallotto; Tom A. Graaf; Caroline Heugten; Alexander T. Sack; Teresa Schuhmann Transcranial magnetic stimulation over posterior parietal cortex modulates alerting and executive control processes in attention Journal Article In: European Journal of Neuroscience, vol. 56, pp. 5853–5868, 2022. @article{MiddagvanSpanje2022, Attention includes three different functional components: generating and maintaining an alert state (alerting), orienting to sensory events (orienting), and resolving conflicts between alternative actions (executive control). Neuroimaging and patient studies suggest that the posterior parietal cortex (PPC) is involved in all three attention components. Transcranial magnetic stimulation (TMS) has repeatedly been applied over the PPC to study its functional role for shifts and maintenance of visuospatial attention. Most TMS-PPC studies used only detection tasks or orienting paradigms to investigate TMS-PPC effects on attention processes, neglecting the alerting and executive control components of attention. The objective of the present study was to investigate the role of PPC in all three functional components of attention: alerting, orienting, and executive control. To this end, we disrupted PPC with TMS (continuous theta-burst stimulation), to modulate subsequent performance on the Lateralized-Attention Network Test, used to assess the three attention components separately. Our results revealed hemifield-specific effects on alerting and executive control functions, but we did not find stimulation effects on orienting performance. While this field of research and associated clinical development have been predominantly focused on orienting performance, our results suggest that parietal cortex and its modulation may affect other aspects of attention as well. |
Soukayna Bekkali; George J. Youssef; Peter H. Donaldson; Jason He; Michael Do; Christian Hyde; Pamela Barhoun; Peter G. Enticott Do gaze behaviours during action observation predict interpersonal motor resonance? Journal Article In: Social Cognitive and Affective Neuroscience, vol. 17, no. 1, pp. 61–71, 2022. @article{Bekkali2022, Interpersonal motor resonance (IMR) is a common putative index of the mirror neuron system (MNS), a network containing specialised cells that fire during both action execution and observation. Visual content inputs to the MNS, however, it is unclear whether visual behaviours mediate the putative MNS response. We aimed to examine gaze effects on IMR during action observation. Neurotypical adults (N = 99; 60 female) underwent transcranial magnetic stimulation, electromyography, and eye-tracking during the observation of videos of actors performing grasping actions. IMR was measured as a percentage change in motor evoked potentials (MEPs) of the first dorsal interosseous muscle during action observation relative to baseline. MEP facilitation was observed during action observation, indicating IMR (65.43% |
Lorenzo Diana; Giulia Scotti; Edoardo N. Aiello; Patrick Pilastro; Aleksandra K. Eberhard-Moscicka; René M. Müri; Nadia Bolognini In: Brain Sciences, vol. 12, pp. 1–20, 2022. @article{Diana2022, Transcranial Direct Current Stimulation (tDCS) has been employed to modulate visuo- spatial attentional asymmetries, however, further investigation is needed to characterize tDCS- associated variability in more ecological settings. In the present research, we tested the effects of offline, anodal conventional tDCS (Experiment 1) and HD-tDCS (Experiment 2) delivered over the posterior parietal cortex (PPC) and Frontal Eye Field (FEF) of the right hemisphere in healthy participants. Attentional asymmetries were measured by means of an eye tracking-based, ecological paradigm, that is, a Free Visual Exploration task of naturalistic pictures. Data were analyzed from a spatiotemporal perspective. In Experiment 1, a pre-post linear mixed model (LMM) indicated a leftward attentional shift after PPC tDCS; this effect was not confirmed when the individual baseline performance was considered. In Experiment 2, FEF HD-tDCS was shown to induce a significant leftward shift of gaze position, which emerged after 6 s of picture exploration and lasted for 200 ms. The present results do not allow us to conclude on a clear efficacy of offline conventional tDCS and HD- tDCS in modulating overt visuospatial attention in an ecological setting. Nonetheless, our findings highlight a complex relationship among stimulated area, focality of stimulation, spatiotemporal aspects of deployment of attention, and the role of individual baseline performance in shaping the effects of tDCS. |
Stefano Gallotto; Teresa Schuhmann; Felix Duecker; Marij Middag-van Spanje; Tom A. Graaf; Alexander T. Sack Concurrent frontal and parietal network TMS for modulating attention Journal Article In: iScience, vol. 25, pp. 1–14, 2022. @article{Gallotto2022, Transcranial magnetic stimulation (TMS) has been applied to frontal eye field (FEF) and intraparietal sulcus (IPS) in isolation, to study their role in attention. However, these nodes closely interact in a “dorsal attention network”. Here, we compared effects of inhibitory TMS applied to individually fMRI-localized FEF or IPS (single-node TMS), to effects of simultaneously inhibiting both regions (“network TMS”), and sham. We assessed attention performance using the lateralized attention network test, which captures multiple facets of attention: spatial orienting, alerting, and executive control. TMS showed no effects on alerting and executive control. For spatial orienting, only network TMS showed a reduction of the orienting effect in the right hemifield compared to the left hemifield, irrespective of the order of TMS application (IPS→FEF or FEF→IPS). Network TMS might prevent compensatory mechanisms within a brain network, which is promising for both research and clinical applications to achieve superior neuromodulation effects. |
Adam M. McNeill; Rebecca L. Monk; Adam W. Qureshi; Stergios Makris; Valentina Cazzato; Derek Heim In: Cognitive, Affective and Behavioral Neuroscience, vol. 22, pp. 160–170, 2022. @article{McNeill2022, Previous research indicates that following alcohol intoxication, activity in prefrontal cortices is reduced, linking to changes in associated cognitive processes, such as inhibitory control, attentional bias (AB), and craving. While these changes have been implicated in alcohol consumption behaviour, it has yet to be fully illuminated how these frontal regions and cognitive processes interact to govern alcohol consumption behaviour. The current preregistered study applied continuous theta burst transcranial magnetic stimulation (cTBS) to examine directly these relationships while removing the wider pharmacological effects of alcohol. A mixed design was implemented, with cTBS stimulation to right and left dorsolateral prefrontal cortex (DLPFC), the medial orbital frontal cortex (mOFC) and Vertex, with measures of inhibitory control, AB, and craving taken both pre- and post-stimulation. Ad libitum consumption was measured using a bogus taste task. Results suggest that rDLPFC stimulation impaired inhibitory control but did not significantly increase ad libitum consumption. However, lDLPFC stimulation heightened craving and increased consumption, with findings indicating that changes in craving partially mediated the relationship between cTBS stimulation ofprefrontal regions and ad libitum consumption. Medial OFC stimulation and AB findings were inconclusive. Overall, results implicate the left DLPFC in the regulation of craving, which appears to be a prepotent cognitive mechanism by which alcohol consumption is driven and maintained. |
Paola Mengotti; Anne Sophie Käsbauer; Gereon R. Fink; Simone Vossel In: Cerebral Cortex, vol. 32, pp. 4698–4714, 2022. @article{Mengotti2022, Updating beliefs after unexpected events is fundamental for an optimal adaptation to the environment. Previous findings suggested a causal involvement of the right temporoparietal junction (rTPJ) in belief updating in an attention task. We combined offline continuous theta-burst stimulation (cTBS) over rTPJ with functional magnetic resonance imaging (fMRI) to investigate local and remote stimulation effects within the attention and salience networks. In a sham-controlled, within-subject crossover design, 25 participants performed an attentional cueing task during fMRI with true or false information about cue predictability. By estimating learning rates from response times, we characterized participants' belief updating. Model-derived cue predictability entered the fMRI analysis as a parametric regressor to identify the neural correlates of updating. rTPJ-cTBS effects showed high interindividual variability. The expected learning rate reduction with false cue predictability information by cTBS was only observed in participants showing higher updating in false than in true blocks after sham. cTBS modulated the neural signatures of belief updating, both in rTPJ and in nodes of the attention and salience networks. The interindividual variability of the behavioral cTBS effect was related to differential activity and rTPJ connectivity of the right anterior insula. These results demonstrate a crucial interaction between ventral attention and salience networks for belief updating. |
Johannes Rennig; Michael S. Beauchamp Intelligibility of audiovisual sentences drives multivoxel response patterns in human superior temporal cortex Journal Article In: NeuroImage, vol. 247, pp. 1–9, 2022. @article{Rennig2022, Regions of the human posterior superior temporal gyrus and sulcus (pSTG/S) respond to the visual mouth movements that constitute visual speech and the auditory vocalizations that constitute auditory speech, and neural responses in pSTG/S may underlie the perceptual benefit of visual speech for the comprehension of noisy auditory speech. We examined this possibility through the lens of multivoxel pattern responses in pSTG/S. BOLD fMRI data was collected from 22 participants presented with speech consisting of English sentences presented in five different formats: visual-only; auditory with and without added auditory noise; and audiovisual with and without auditory noise. Participants reported the intelligibility of each sentence with a button press and trials were sorted post-hoc into those that were more or less intelligible. Response patterns were measured in regions of the pSTG/S identified with an independent localizer. Noisy audiovisual sentences with very similar physical properties evoked very different response patterns depending on their intelligibility. When a noisy audiovisual sentence was reported as intelligible, the pattern was nearly identical to that elicited by clear audiovisual sentences. In contrast, an unintelligible noisy audiovisual sentence evoked a pattern like that of visual-only sentences. This effect was less pronounced for noisy auditory-only sentences, which evoked similar response patterns regardless of intelligibility. The successful integration of visual and auditory speech produces a characteristic neural signature in pSTG/S, highlighting the importance of this region in generating the perceptual benefit of visual speech. |
2021 |
Delia A. Gheorghe; Muriel T. N. Panouillères; Nicholas D. Walsh Investigating the effects of cerebellar transcranial direct current stimulation on saccadic adaptation and cortisol response Journal Article In: Cerebellum and Ataxias, vol. 8, no. 1, pp. 1–11, 2021. @article{Gheorghe2021, Background: Transcranial Direct Current Stimulation (tDCS) over the prefrontal cortex has been shown to modulate subjective, neuronal and neuroendocrine responses, particularly in the context of stress processing. However, it is currently unknown whether tDCS stimulation over other brain regions, such as the cerebellum, can similarly affect the stress response. Despite increasing evidence linking the cerebellum to stress-related processing, no studies have investigated the hormonal and behavioural effects of cerebellar tDCS. Methods: This study tested the hypothesis of a cerebellar tDCS effect on mood, behaviour and cortisol. To do this we employed a single-blind, sham-controlled design to measure performance on a cerebellar-dependent saccadic adaptation task, together with changes in cortisol output and mood, during online anodal and cathodal stimulation. Forty-five participants were included in the analysis. Stimulation groups were matched on demographic variables, potential confounding factors known to affect cortisol levels, mood and a number of personality characteristics. Results: Results showed that tDCS polarity did not affect cortisol levels or subjective mood, but did affect behaviour. Participants receiving anodal stimulation showed an 8.4% increase in saccadic adaptation, which was significantly larger compared to the cathodal group (1.6%). Conclusion: The stimulation effect on saccadic adaptation contributes to the current body of literature examining the mechanisms of cerebellar stimulation on associated function. We conclude that further studies are needed to understand whether and how cerebellar tDCS may module stress reactivity under challenge conditions. |
Lara Merken; Marco Davare; Peter Janssen; Maria C. Romero Behavioral effects of continuous theta-burst stimulation in macaque parietal cortex Journal Article In: Scientific Reports, vol. 11, pp. 4511, 2021. @article{Merken2021, The neural mechanisms underlying the effects of continuous Theta-Burst Stimulation (cTBS) in humans are poorly understood. Animal studies can clarify the effects of cTBS on individual neurons, but behavioral evidence is necessary to demonstrate the validity of the animal model. We investigated the behavioral effect of cTBS applied over parietal cortex in rhesus monkeys performing a visually-guided grasping task with two differently sized objects, which required either a power grip or a pad-to-side grip. We used Fitts' law, predicting shorter grasping times (GT) for large compared to small objects, to investigate cTBS effects on two different grip types. cTBS induced long-lasting object-specific and dose-dependent changes in GT that remained present for up to two hours. High-intensity cTBS increased GTs for a power grip, but shortened GTs for a pad-to-side grip. Thus, high-intensity stimulation strongly reduced the natural GT difference between objects (i.e. the Fitts' law effect). In contrast, low-intensity cTBS induced the opposite effects on GT. Modifying the coil orientation from the standard 45-degree to a 30-degree angle induced opposite cTBS effects on GT. These findings represent behavioral evidence for the validity of the nonhuman primate model to study the neural underpinnings of non-invasive brain stimulation. |
Kentaro Miyamoto; Nadescha Trudel; Kevin Kamermans; Michele C. Lim; Alberto Lazari; Lennart Verhagen; Marco K. Wittmann; Matthew F. S. Rushworth Identification and disruption of a neural mechanism for accumulating prospective metacognitive information prior to decision-making Journal Article In: Neuron, vol. 109, no. 8, pp. 1396–1408, 2021. @article{Miyamoto2021, More than one type of probability must be considered when making decisions. It is as necessary to know one's chance of performing choices correctly as it is to know the chances that desired outcomes will follow choices. We refer to these two choice contingencies as internal and external probability. Neural activity across many frontal and parietal areas reflected internal and external probabilities in a similar manner during decision-making. However, neural recording and manipulation approaches suggest that one area, the anterior lateral prefrontal cortex (alPFC), is highly specialized for making prospective, metacognitive judgments on the basis of internal probability; it is essential for knowing which decisions to tackle, given its assessment of how well they will be performed. Its activity predicted prospective metacognitive judgments, and individual variation in activity predicted individual variation in metacognitive judgments. Its disruption altered metacognitive judgments, leading participants to tackle perceptual decisions they were likely to fail. |
Guanpeng Chen; Ziyun Zhu; Qing He; Fang Fang Offline transcranial direct current stimulation improves the ability to perceive crowded targets Journal Article In: Journal of Vision, vol. 21, no. 2, pp. 1–10, 2021. @article{Chen2021a, The deleterious effect of nearby flankers on target identification in the periphery is known as visual crowding. Studying visual crowding can advance our understanding of the mechanisms of visual awareness and object recognition. Alleviating visual crowding is one of the major ways to improve peripheral vision. The aim of the current study was to examine whether transcranial direct current stimulation (tDCS) was capable of alleviating visual crowding at different visual eccentricities and with different visual tasks. In the present single-blind sham-controlled study, subjects were instructed to perform an orientation discrimination task or a letter identification task with isolated and crowded targets in the periphery, before and after applying 20 minutes of 2 mA anodal tDCS to visual cortex of the hemisphere contralateral or ipsilateral to visual stimuli. Contralateral tDCS significantly alleviated the orientation crowding effect at two different eccentricities and the letter crowding effect. This alleviation was absent after sham or ipsilateral stimulation and could not be fully explained by the performance improvement with the isolated targets. These findings demonstrated that offline tDCS was effective in alleviating visual crowding across different visual eccentricities and tasks, therefore providing a promising way to improve spatial vision rapidly in crowded scenes. |
Andra Coldea; Stephanie Morand; Domenica Veniero; Monika Harvey; Gregor Thut Parietal alpha tACS shows inconsistent effects on visuospatial attention Journal Article In: PLoS ONE, vol. 16, no. 8, pp. e0255424, 2021. @article{Coldea2021, Transcranial alternating current stimulation (tACS) is a popular technique that has been used for manipulating brain oscillations and inferring causality regarding the brain-behaviour relationship. Although it is a promising tool, the variability of tACS results has raised questions regarding the robustness and reproducibility of its effects. Building on recent research using tACS to modulate visuospatial attention, we here attempted to replicate findings of lateralized parietal tACS at alpha frequency to induce a change in attention bias away from the contra- towards the ipsilateral visual hemifield. 40 healthy participants underwent tACS in two separate sessions where either 10 Hz tACS or sham was applied via a high-density montage over the left parietal cortex at 1.5 mA for 20 min, while performance was assessed in an endogenous attention task. Task and tACS parameters were chosen to match those of previous studies reporting positive effects. Unlike these studies, we did not observe lateralized parietal alpha tACS to affect attention deployment or visual processing across the hemifields as compared to sham. Likewise, additional resting electroencephalography immediately offline to tACS did not reveal any notable effects on individual alpha power or frequency. Our study emphasizes the need for more replication studies and systematic investigations of the factors that drive tACS effects. |
Raymundo Machado Azevedo Neto; Andreas Bartels Disrupting short-term memory maintenance in premotor cortex affects serial dependence in visuomotor integration Journal Article In: Journal of Neuroscience, vol. 41, no. 45, pp. 9392–9402, 2021. @article{deAzevedoNeto2021, Human behavior is biased by past experience. For example, when intercepting a moving target, the speed of previous targets will bias responses in future trials. Neural mechanisms underlying this so-called serial dependence are still under debate. Here, we tested the hypothesis that the previous trial leaves a neural trace in brain regions associated with encoding task-relevant information in visual and/or motor regions. We reasoned that injecting noise by means of transcranial magnetic stimulation (TMS) over premotor and visual areas would degrade such memory traces and hence reduce serial dependence. To test this hypothesis, we applied bursts of TMS pulses to right visual motion processing region hV5/MT1 and to left dorsal premotor cortex (PMd) during intertrial intervals of a coincident timing task performed by twenty healthy human participants (15 female). Without TMS, participants presented a bias toward the speed of the previous trial when intercepting moving targets. TMS over PMd decreased serial dependence in comparison to the control Vertex stimulation, whereas TMS applied over hV5/MT1 did not. In addition, TMS seems to have specifically affected the memory trace that leads to serial dependence, as we found no evidence that participants' behavior worsened after applying TMS. These results provide causal evidence that an implicit short-term memory mechanism in premotor cortex keeps information from one trial to the next, and that this information is blended with current trial information so that it biases behavior in a visuomotor integration task with moving objects. |
P. J. Hills; G. Arabacı; J. Fagg; L. Canter; C. Thompson; R. Moseley Low-frequency rTMS to the parietal lobe increases eye-movement carryover and decreases hazard rating Journal Article In: Neuropsychologia, vol. 158, pp. 107895, 2021. @article{Hills2021, The persistence of attentional set from one task to a secondary unrelated task, revealed through carryover of eye movements, has been attributed to increased activation in the parietal lobe and decreased activation to the frontal lobe. To directly test this, we adopted a modified version of the Thompson and Crundall (2011) paradigm using low-frequency repetitive TMS to P3 and F3. In each trial, participants viewed letter-strings that were arranged horizontally, vertically, or randomly across the screen before viewing a road image and providing a hazardousness rating for it. The orientation of the letter search influenced eye movements to the road images and this carryover was greater following stimulation to F3 than to P3 (or sham). Furthermore, hazardous ratings were lower following P3 stimulation. These results confirm the involvement of attentional orienting and switching mechanisms in the carryover of eye movements. It is suggested that this “attentional inertia” effect will increase with greater orienting of attentional resources in an initial task and poor inhibition of previously-relevant settings between tasks. |
Tzu-Yu Hsu; Jui-Tai Chen; Philip Tseng; Chin-An Wang Role of the frontal eye field in human microsaccade responses: A TMS study Journal Article In: Biological Psychology, vol. 165, pp. 108202, 2021. @article{Hsu2021, Microsaccade is a type of fixational eye movements that is modulated by various sensory and cognitive processes, and impact our visual perception. Although studies in monkeys have demonstrated a functional role for the superior colliculus and frontal eye field (FEF) in controlling microsaccades, our understanding of the neural mechanisms underlying the generation of microsaccades is still limited. By applying continuous theta-burst stimulation (cTBS) over the right FEF and the vertex, we investigated the role of the FEF in generating human microsaccade responses evoked by salient stimuli or by changes in background luminance. We observed higher microsaccade rates prior to target appearance, and larger rebound in microsaccade occurrence following salient stimuli, when disruptive cTBS was applied over FEF compared to vertex stimulation. Moreover, the microsaccade direction modulation after changes in background luminance was disrupted with FEF stimulation. Together, our results constitute the first evidence of FEF modulation in human microsaccade responses. |
Tzu-Yu Hsu; Yu-Fan Hsu; Hsin-Yi Wang; Chin-An Wang Role of the frontal eye field in human pupil and saccade orienting responses Journal Article In: European Journal of Neuroscience, vol. 54, no. 1, pp. 4283–4294, 2021. @article{Hsu2021a, The appearance of a salient stimulus evokes a series of orienting responses including saccades and pupil size to prepare the body for appropriate action. The midbrain superior colliculus (SC) that receives critical control signals from the frontal eye field (FEF) is hypothesized to coordinate all components of orienting. It has shown recently that the FEF, together with the SC, is also importantly involved in the control of pupil size, in addition to its well-documented role in eye movements. Although the role of the FEF in pupil size is demonstrated in monkeys, its role in human pupil responses and the coordination between pupil size and saccades remains to be established. Through applying continuous theta-burst stimulation over the right FEF and vertex, we investigated the role of the FEF in human pupil and saccade responses evoked by a salient stimulus, and the coordination between pupil size and saccades. Our results showed that neither saccade reaction times (SRT) nor pupil responses evoked by salient stimuli were modulated by FEF stimulation. In contrast, the correlation between pupil size and SRTs in the contralateral stimulus condition was diminished with FEF stimulation, but intact with vertex stimulation. Moreover, FEF stimulation effects between saccade and pupil responses associated with salient stimuli correlated across participants. This is the first transcranial magnetic stimulation (TMS) study on the pupil orienting response, and our findings suggest that human FEF was involved in coordinating pupil size and saccades, but not involved in the control of pupil orienting responses. |
Zhenlan Jin; Ruie Gou; Junjun Zhang; Ling Li The role of frontal pursuit area in interaction between smooth pursuit eye movements and attention: A TMS study Journal Article In: Journal of Vision, vol. 21, no. 3, pp. 1–10, 2021. @article{Jin2021, Close coupling between attention and smooth pursuit eye movements has been widely established and frontal eye field (FEF) is a “hub” region for attention and eye movements. Frontal pursuit area (FPA), a subregion of the FEF, is part of neural circuit for the pursuit, here, we directly checked the role of the FPA in the interaction between the pursuit and attention. To do it, we applied a dual-task paradigm where an attention demanding task was integrated into the pursuit target and interrupted the FPA using transcranial magnetic stimulation (TMS). In the study, participants were required to pursue a moving circle with a letter inside, which changed to another one every 100 ms and report whether “H” (low attentional load) or one of “H,” “S,” or “L” (high attentional load) appeared during the trial. As expected, increasing the attentional load decreased accuracy of the letter detection. Importantly, the FPA TMS had no effect on both the pursuit and letter detection tasks in the low load condition, whereas it reduced 200 to 320 ms gain, but tended to increase the letter detection accuracy in the high load condition. Moreover, individual's FPA TMS effect on pursuit gain |
Björn Machner; Jonathan Imholz; Lara Braun; Philipp J. Koch; Tobias Bäumer; Thomas F. Münte; Christoph Helmchen; Andreas Sprenger In: Neuroimage: Reports, vol. 1, no. 2, pp. 100013, 2021. @article{Machner2021, Disruption of resting-state functional connectivity (RSFC) between core regions of the dorsal attention network (DAN), including the bilateral superior parietal lobule (SPL), and structural damage of the right-lateralized ventral attention network (VAN), including the temporo-parietal junction (TPJ), have been described as neural basis for hemispatial neglect. Pursuing a virtual lesion model, we aimed to perturbate the attention networks of 22 healthy subjects by applying continuous theta burst stimulation (cTBS) to the right SPL or TPJ. We first created network masks of the DAN and VAN based on RSFC analyses from a RS-fMRI baseline session and determined the SPL and TPJ stimulation site within the respective mask. We then performed RS-fMRI immediately after cTBS of the SPL, TPJ (active sites) or vertex (control site). RSFC between SPL/TPJ and whole brain as well as between predefined regions of interest (ROI) in the attention networks was analyzed in a within-subject design. Contrary to our hypothesis, seed-based RSFC did not differ between the four experimental conditions. The individual change in ROI-to-ROI RSFC from baseline to post-stimulation did also not differ between active (SPL, TPJ) and control (vertex) cTBS. In our study, a single session offline cTBS over the right SPL or TPJ could not alter RSFC in the attention networks as compared to a control stimulation, maybe because effects wore off too early. Future studies should consider a modified cTBS protocol, concurrent TMS-fMRI or transcranial direct current stimulation. |
Roberto F. Salanamca-Giron; Estelle Raffin; Sarah B. Zandvliet; Martin Seeber; Christoph M. Michel; Paul Sauseng; Krystel R. Huxlin; Friedhelm C. Hummel Enhancing visual motion discrimination by desynchronizing bifocal oscillatory activity Journal Article In: NeuroImage, vol. 240, pp. 118299, 2021. @article{SalanamcaGiron2021, Visual motion discrimination involves reciprocal interactions in the alpha band between the primary visual cortex (V1) and mediotemporal areas (V5/MT). We investigated whether modulating alpha phase synchronization using individualized multisite transcranial alternating current stimulation (tACS) over V5 and V1 regions would improve motion discrimination. We tested 3 groups of healthy subjects with the following conditions: (1) individualized In-Phase V1alpha-V5alpha tACS (0° lag), (2) individualized Anti-Phase V1alpha-V5alpha tACS (180° lag) and (3) sham tACS. Motion discrimination and EEG activity were recorded before, during and after tACS. Performance significantly improved in the Anti-Phase group compared to the In-Phase group 10 and 30 min after stimulation. This result was explained by decreases in bottom-up alpha-V1 gamma-V5 phase-amplitude coupling. One possible explanation of these results is that Anti-Phase V1alpha-V5alpha tACS might impose an optimal phase lag between stimulation sites due to the inherent speed of wave propagation, hereby supporting optimized neuronal communication. |
Omer Sharon; Firas Fahoum; Yuval Nir Transcutaneous vagus nerve stimulation in humans induces pupil dilation and attenuates alpha oscillations Journal Article In: Journal of Neuroscience, vol. 41, no. 2, pp. 320–330, 2021. @article{Sharon2021, Vagus nerve stimulation (VNS) is widely used to treat drug-resistant epilepsy and depression. While the precise mechanisms mediating its long-term therapeutic effects are not fully resolved, they likely involve locus coeruleus (LC) stimulation via the nucleus of the solitary tract, which receives afferent vagal inputs. In rats, VNS elevates LC firing and forebrain noradrenaline levels, whereas LC lesions suppress VNS therapeutic efficacy. Noninvasive transcutaneous VNS (tVNS) uses electrical stimulation that targets the auricular branch of the vagus nerve at the cymba conchae of the ear. However, the extent to which tVNS mimics VNS remains unclear. Here, we investigated the short-term effects of tVNS in healthy human male volunteers (n = 24), using high-density EEG and pupillometry during visual fixation at rest. We compared short (3.4 s) trials of tVNS to sham electrical stimulation at the earlobe (far from the vagus nerve branch) to control for somatosensory stimulation. Although tVNS and sham stimulation did not differ in subjective intensity ratings, tVNS led to robust pupil dilation (peaking 4-5 s after trial onset) that was significantly higher than following sham stimulation. We further quantified, using parallel factor analysis, how tVNS modulates idle occipital alpha (8-13Hz) activity identified in each participant. We found greater attenuation of alpha oscillations by tVNS than by sham stimulation. This demonstrates that tVNS reliably induces pupillary and EEG markers of arousal beyond the effects of somatosensory stimulation, thus supporting the hypothesis that tVNS elevates noradrenaline and other arousal-promoting neuromodulatory signaling, and mimics invasive VNS. |
Chloé Stengel; Marine Vernet; Julià L. Amengual; Antoni Valero-Cabré In: Scientific Reports, vol. 11, pp. 3807, 2021. @article{Stengel2021, Correlational evidence in non-human primates has reported increases of fronto-parietal high-beta (22–30 Hz) synchrony during the top-down allocation of visuo-spatial attention. But may inter-regional synchronization at this specific frequency band provide a causal mechanism by which top-down attentional processes facilitate conscious visual perception? To address this question, we analyzed electroencephalographic (EEG) signals from a group of healthy participants who performed a conscious visual detection task while we delivered brief (4 pulses) rhythmic (30 Hz) or random bursts of Transcranial Magnetic Stimulation (TMS) to the right Frontal Eye Field (FEF) prior to the onset of a lateralized target. We report increases of inter-regional synchronization in the high-beta band (25–35 Hz) between the electrode closest to the stimulated region (the right FEF) and right parietal EEG leads, and increases of local inter-trial coherence within the same frequency band over bilateral parietal EEG contacts, both driven by rhythmic but not random TMS patterns. Such increases were accompained by improvements of conscious visual sensitivity for left visual targets in the rhythmic but not the random TMS condition. These outcomes suggest that high-beta inter-regional synchrony can be modulated non-invasively and that high-beta oscillatory activity across the right dorsal fronto-parietal network may contribute to the facilitation of conscious visual perception. Our work supports future applications of non-invasive brain stimulation to restore impaired visually-guided behaviors by operating on top-down attentional modulatory mechanisms. |
2020 |
Ian G. M. Cameron; Andreea Cretu; Femke Struik; Ivan Toni The effects of a TMS double lesion to a cortical network Journal Article In: eNeuro, vol. 7, no. 1, pp. 1–22, 2020. @article{Cameron2020, Transcranial magnetic stimulation (TMS) is often used to understand the function of individual brain regions, but this ignores the fact that TMS may affect network-level rather than nodal-level processes. We examine the effects from a “double lesion” to two frontoparietal network nodes compared to the effects from single lesions to either node. We hypothesize that the absence of additive effects indicates that a single lesion is consequential to a network-level process. Twenty-three humans performed pro- (look towards) and anti- (look away) saccades after receiving continuous theta-burst stimulation (cTBS) to right frontal eye fields (FEF), dorsolateral prefrontal cortex (DLPFC) or somatosensory cortex (S1) (the control region). On a subset of trials, a TMS pulse was applied to right posterior parietal cortex (PPC). FEF, DLPFC and PPC are important frontoparietal network nodes for controlling anti-saccades. Bayesian T-tests were used to test hypotheses for additive double lesion effects on saccade behaviors (cTBS plus TMS pulse) against the null hypothesis that double lesion effects are not different than single lesion effects. We observed strong evidence (BF10 = 325.22) that DLPFC cTBS plus PPC TMS lesion enhanced impairments in ipsilateral anti-saccade amplitudes over DLPFC cTBS alone, but not over the effect of the PPC pulse alone (BF10 = 0.75). Therefore, effects were not additive, and no other evidence for additive effects was found (BF10 < 3). This suggests that saccade-control computations are distributed across this network, with some degree of compensation by PPC for the DLPFC lesion. |
Ian M. Erkelens; William R. Bobier; Alicia C. Macmillan; Nicole L. Maione; Claudia Martin Calderon; Heidi Patterson; Benjamin Thompson A differential role for the posterior cerebellum in the adaptive control of convergence eye movements Journal Article In: Brain Stimulation, vol. 13, no. 1, pp. 215–228, 2020. @article{Erkelens2020a, Introduction: The vergence oculomotor system possesses two robust adaptive mechanisms; a fast “dynamic” and a slow “tonic” system that are both vital for single, clear and comfortable binocular vision. The neural substrates underlying these vergence adaptive mechanisms in humans is unclear. Methods: We investigated the role of the posterior cerebellum in convergence adaptation using inhibitory continuous theta-burst repetitive transcranial magnetic stimulation (cTBS) within a double-blind, sham controlled design while eye movements were recorded at 250hz via infrared oculography. Results: In a preliminary experiment we validated our stimulation protocols by reproducing results from previous work on saccadic adaptation during the classic double-step adaptive shortening paradigm. Following this, across a series of three separate experiments we observed a clear dissociation in the effect of cTBS on convergence adaptation. Dynamic adaptation was substantially reduced while tonic adaptation was unaffected. Baseline dynamic fusional vergence response were also unaffected by stimulation. Conclusions: These results indicate a differential role for the posterior cerebellum in the adaptive control of convergence eye movements and provide initial evidence that repetitive transcranial magnetic stimulation is a viable tool to investigate the neurophysiology of vergence control. The results are discussed in the context of the current models of implicit motor adaptation of vergence and their application to clinical populations and technology design in virtual and augmented head mounted display architectures. Significance statement: The cerebellum plays a critical role in the adaptive control of motor systems. Vergence eye movements shift our gaze in depth allowing us to see in 3D and exhibit two distinct adaptive mechanisms that are engaged under a range of conditions including reading, wearing head-mounted displays and using a new spectacle prescription. It is unclear what role the cerebellum plays in these adaptive mechanisms. To answer this, we temporarily disrupted the function of the posterior cerebellum using non-invasive brain stimulation and report impairment of only one adaptive mechanism, providing evidence for neural compartmentalization. The results have implications for vergence control models and applications to comfort and experience studies in head-mounted displays and the rehabilitation of clinical populations exhibiting vergence dysfunctions. |
Antonio Fernández; Marisa Carrasco Extinguishing exogenous attention via transcranial magnetic stimulation Journal Article In: Current Biology, vol. 30, no. 20, pp. 4078–4084, 2020. @article{Fernandez2020, Orienting covert exogenous (involuntary) attention to a target location improves performance in many visual tasks [1, 2]. It is unknown whether early visual cortical areas are necessary for this improvement. To establish a causal link between these areas and attentional modulations, we used transcranial magnetic stimulation (TMS) to briefly alter cortical excitability and determine whether early visual areas mediate the effect of exogenous attention on performance. Observers performed an orientation discrimination task. After a peripheral valid, neutral, or invalid cue, two cortically magnified gratings were presented, one in the stimulated region and the other in the symmetric region in the opposite hemifield. Observers received two successive TMS pulses around their occipital pole while the stimuli were presented. Shortly after, a response cue indicated the grating whose orientation observers had to discriminate. The response cue either matched—target stimulated—or did not match—distractor stimulated—the stimulated side. Grating contrast was varied to measure contrast response functions (CRF) for all combinations of attention and TMS conditions. When the distractor was stimulated, exogenous attention yielded response gain—performance benefits in the valid-cue condition and costs in the invalid-cue condition compared with the neutral condition at the high contrast levels. Crucially, when the target was stimulated, this response gain was eliminated. Therefore, TMS extinguished the effect of exogenous attention. These results establish a causal link between early visual areas and the modulatory effect of exogenous attention on performance. |
Eric B. Knudsen; Joni D. Wallis Closed-loop theta stimulation in the orbitofrontal cortex prevents reward-based learning Journal Article In: Neuron, vol. 106, no. 3, pp. 537–547.e4, 2020. @article{Knudsen2020, Although neuronal oscillations correlate with many high-level cognitive processes, their causal contribution is less clear. Using a novel closed-loop microstimulation protocol, Knudsen and Wallis demonstrate the necessity of theta oscillations in the orbitofrontal cortex for reward-based learning. |
Pierre Pouget; Stephen Frey; Harry Ahnine; David Attali; Julien Claron; Charlotte Constans; Jean-Francois Aubry; Fabrice Arcizet In: Frontiers in Physiology, vol. 11, pp. 1042, 2020. @article{Pouget2020, Since the late 2010s, Transcranial Ultrasound Stimulation (TUS) has been used experimentally to carryout safe, non-invasive stimulation of the brain with better spatial resolution than Transcranial Magnetic Stimulation (TMS). This innovative stimulation method has emerged as a novel and valuable device for studying brain function in humans and animals. In particular, single pulses of TUS directed to oculomotor regions have been shown to modulate visuomotor behavior of non-human primates during 100 ms ultrasound pulses. In the present study, a sustained effect was induced by applying 20-s trains of neuronavigated repetitive Transcranial Ultrasound Stimulation (rTUS) to oculomotor regions of the frontal cortex in three non-human primates performing an antisaccade task. With the help of MRI imaging and a frame-less stereotactic neuronavigation system (SNS), we were able to demonstrate that neuronavigated TUS (outside of the MRI scanner) is an efficient tool to carry out neuromodulation procedures in non-human primates. We found that, following neuronavigated rTUS, saccades were significantly modified, resulting in shorter latencies compared to no-rTUS trials. This behavioral modulation was maintained for up to 20 min. Oculomotor behavior returned to baseline after 18–31 min and could not be significantly distinguished from the no-rTUS condition. This study is the first to show that neuronavigated rTUS can have a persistent effect on monkey behavior with a quantified return-time to baseline. The specificity of the effects could not be explained by auditory confounds. |
David Zeugin; Michael P. Notter; Jean François Knebel; Silvio Ionta Temporo-parietal contribution to the mental representations of self/other face Journal Article In: Brain and Cognition, vol. 143, pp. 1–6, 2020. @article{Zeugin2020, Face recognition requires comparing the current visual input with stored mental representations of faces. Based on its role in visual recognition of faces and mental representation of the body, we hypothesized that the right temporo-parietal junction (rTPJ) could be implicated also in processing mental representation of faces. To test this hypothesis, we asked 30 neurotypical participants to perform mental rotation (laterality judgment of rotated pictures) of self- and other-face images, before and after the inhibition of rTPJ through repetitive transcranial magnetic stimulation. After inhibition of rTPJ the mental rotation of self-face was slower than other-face. In the control condition the mental rotation of self/other faces was not significantly different. This supports that the role of rTPJ extends to mental representation of faces, specifically for the self. Since the experimental task did not require to explicitly recognize identity, we propose that unconscious identity attribution affects also the mental representation of faces. The present study offers insights on the involvement rTPJ in mental representation of faces and proposes that the neural substrate dedicated to mental representation of faces goes beyond the traditional visual and memory areas. |
2019 |
Maria C. Romero; Marco Davare; Marcelo Armendariz; Peter Janssen Neural effects of transcranial magnetic stimulation at the single-cell level Journal Article In: Nature Communications, vol. 10, pp. 2642, 2019. @article{Romero2019, Transcranial magnetic stimulation (TMS) can non-invasively modulate neural activity in humans. Despite three decades of research, the spatial extent of the cortical area activated by TMS is still controversial. Moreover, how TMS interacts with task-related activity during motor behavior is unknown. Here, we applied single-pulse TMS over macaque parietal cortex while recording single-unit activity at various distances from the center of stimulation during grasping. The spatial extent of TMS-induced activation is remarkably restricted, affecting the spiking activity of single neurons in an area of cortex measuring less than 2 mm in diameter. In task-related neurons, TMS evokes a transient excitation followed by reduced activity, paralleled by a significantly longer grasping time. Furthermore, TMS-induced activity and task-related activity do not summate in single neurons. These results furnish crucial experimental evidence for the neural effects of TMS at the single-cell level and uncover the neural underpinnings of behavioral effects of TMS. |
Nuno Alexandre De Sá Teixeira; Gianfranco Bosco; Sergio Delle Monache; Francesco Lacquaniti In: Experimental Brain Research, vol. 237, no. 12, pp. 3375–3390, 2019. @article{DeSaTeixeira2019, The perceived vanishing location of a moving target is systematically displaced forward, in the direction of motion—representational momentum—, and downward, in the direction of gravity—representational gravity. Despite a wealth of research on the factors that modulate these phenomena, little is known regarding their neurophysiological substrates. The present experiment aims to explore which role is played by cortical areas hMT/V5+, linked to the processing of visual motion, and TPJ, thought to support the functioning of an internal model of gravity, in modulating both effects. Participants were required to perform a standard spatial localization task while the activity of the right hMT/V5+ or TPJ sites was selectively disrupted with an offline continuous theta-burst stimulation (cTBS) protocol, interspersed with control blocks with no stimulation. Eye movements were recorded during all spatial localizations. Results revealed an increase in representational gravity contingent on the disruption of the activity of hMT/V5+ and, conversely, some evidence suggested a bigger representational momentum when TPJ was stimulated. Furthermore, stimulation of hMT/V5+ led to a decreased ocular overshoot and to a time-dependent downward drift of gaze location. These outcomes suggest that a reciprocal balance between perceived kinematics and anticipated dynamics might modulate these spatial localization responses, compatible with a push–pull mechanism. |
Ya Li; Yonghui Wang; Sheng Li Recurrent processing of contour integration in the human visual cortex as revealed by fMRI-guided TMS Journal Article In: Cerebral Cortex, vol. 29, no. 1, pp. 17–26, 2019. @article{Li2019i, Contour integration is a critical step in visual perception because it groups discretely local elements into perceptually global contours. Previous investigations have suggested that striate and extrastriate visual areas are involved in this mid-level processing of visual perception. However, the temporal dynamics of these areas in the human brain during contour integration is less understood. The present study used functional magnetic resonance imaging-guided transcranial magnetic stimulation (TMS) to briefly disrupt 1 of 2 visual areas (V1/V2 and V3B) and examined the causal contributions of these areas to contour detection. The results demonstrated that the earliest critical time window at which behavioral detection performance was impaired by TMS pluses differed between V1/V2 and V3B. The first critical window of V3B (90-110 ms after stimulus onset) was earlier than that of V1/V2 (120-140 ms after stimulus onset), thus indicating that feedback connection from higher to lower area was necessary for complete contour integration. These results suggested that the fine processing of contour-related information in V1/V2 follows the generation of a coarse template in the higher visual areas, such as V3B. Our findings provide direct causal evidence that a recurrent mechanism is necessary for the integration of contours from cluttered background in the human brain. |
Marine Vernet; Chloé Stengel; Romain Quentin; Julià L. Amengual; Antoni Valero-Cabré Entrainment of local synchrony reveals a causal role for high-beta right frontal oscillations in human visual consciousness Journal Article In: Scientific Reports, vol. 9, pp. 14510, 2019. @article{Vernet2019, Prior evidence supports a critical role of oscillatory activity in visual cognition, but are cerebral oscillations simply correlated or causally linked to our ability to consciously acknowledge the presence of a target in our visual field? Here, EEG signals were recorded on humans performing a visual detection task, while they received brief patterns of rhythmic or random transcranial magnetic stimulation (TMS) delivered to the right Frontal Eye Field (FEF) prior to the onset of a lateralized target. TMS entrained oscillations, i.e., increased high-beta power and phase alignment (the latter to a higher extent for rhythmic high-beta patterns than random patterns) while also boosting visual detection sensitivity. Considering post-hoc only those participants in which rhythmic stimulation enhanced visual detection, the magnitude of high-beta entrainment correlated with left visual performance increases. Our study provides evidence in favor of a causal link between high-beta oscillatory activity in the Frontal Eye Field and visual detection. Furthermore, it supports future applications of brain stimulation to manipulate local synchrony and improve or restore impaired visual behaviors. |
2018 |
Thérèse Collins; Pierre O. Jacquet TMS over posterior parietal cortex disrupts trans-saccadic visual stability Journal Article In: Brain Stimulation, vol. 11, no. 2, pp. 390–399, 2018. @article{Collins2018, Background: Saccadic eye movements change the retinal location of visual objects, but we do not experience the visual world as constantly moving, we perceive it as seamless and stable. This visual stability may be achieved by an internal or efference copy of each saccade that, combined with the retinal information, allows the visual system to cancel out or ignore the self-caused retinal motion. Objective: The current study investigated the underlying brain mechanisms responsible for visual stability in humans with online transcranial magnetic stimulation (TMS). Methods: We used two classic tasks that measure efference copy: the double-step task and the in-flight displacement task. The double-step task requires subjects to make two memory-guided saccades, the second of which depends on an accurate internal copy of the first. The in-flight displacement task requires subjects to report the relative location of a (possibly displaced) target across a saccade. In separate experimental sessions, subjects participated in each task while we delivered online 3-pulse TMS over frontal eye fields (FEF), posterior parietal cortex, or vertex. TMS was contingent on saccade execution. Results: Second saccades were not disrupted in the double-step task, but surprisingly, TMS over FEF modified the metrics of the ongoing saccade. Spatiotopic performance in the in-flight displacement task was altered following TMS over parietal cortex, but not FEF or vertex. Conclusion: These results suggest that TMS disrupted eye-centered position coding in the parietal cortex. Trans-saccadic correspondence, and visual stability, may therefore causally depend on parietal maps. |
Seref Can Gurel; Miguel Castelo-Branco; Alexander T. Sack; Felix Duecker Assessing the functional role of frontal eye fields in voluntary and reflexive saccades using continuous theta burst stimulation Journal Article In: Frontiers in Neuroscience, vol. 12, pp. 944, 2018. @article{Gurel2018, The frontal eye fields (FEFs) are core nodes of the oculomotor system contributing to saccade planning, control, and execution. Here, we aimed to reveal hemispheric asymmetries between left and right FEF in both voluntary and reflexive saccades toward horizontal and vertical targets. To this end, we applied fMRI-guided continuous theta burst stimulation (cTBS) over either left or right FEF and assessed the consequences of this disruption on saccade latencies. Using a fully counterbalanced within-subject design, we measured saccade latencies before and after the application of cTBS in eighteen healthy volunteers. In general, saccade latencies on both tasks were susceptible to our experimental manipulations, that is, voluntary saccades were slower than reflexive saccades, and downward saccades were slower than upward saccades. Contrary to our expectations, we failed to reveal any TMS-related effects on saccade latencies, and Bayesian analyses provided strong support in favor of a TMS null result for both tasks. Keeping in mind the interpretative challenges of null results, we discuss possible explanations for this absence of behavioral TMS effects, focusing on methodological differences compared to previous studies (task parameters and online vs. offline TMS interventions). We also speculate about what our results might reveal about the functional role of FEF. |
George L. Malcolm; Edward H. Silson; Jennifer R. Henry; Chris I. Baker Transcranial magnetic stimulation to the occipital place area biases gaze during scene viewing Journal Article In: Frontiers in Human Neuroscience, vol. 12, pp. 189, 2018. @article{Malcolm2018, We can understand viewed scenes and extract task-relevant information within a few hundred milliseconds. This process is generally supported by three cortical regions that show selectivity for scene images: parahippocampal place area (PPA), medial place area (MPA) and occipital place area (OPA). Prior studies have focused on the visual information each region is responsive to, usually within the context of recognition or navigation. Here, we move beyond these tasks to investigate gaze allocation during scene viewing. Eye movements rely on a scene's visual representation to direct saccades, and thus foveal vision. In particular, we focus on the contribution of OPA, which is: (i) located in occipito-parietal cortex, likely feeding information into parts of the dorsal pathway critical for eye movements; and (ii) contains strong retinotopic representations of the contralateral visual field. Participants viewed scene images for 1034 ms while their eye movements were recorded. On half of the trials, a 500 ms train of five transcranial magnetic stimulation (TMS) pulses was applied to the participant's cortex, starting at scene onset. TMS was applied to the right hemisphere over either OPA or the occipital face area (OFA), which also exhibits a contralateral visual field bias but shows selectivity for face stimuli. Participants generally made an overall left-toright, top-to-bottom pattern of eye movements across all conditions. When TMS was applied to OPA, there was an increased saccade latency for eye movements toward the contralateral relative to the ipsilateral visual field after the final TMS pulse (400 ms). Additionally, TMS to the OPA biased fixation positions away from the contralateral side of the scene compared to the control condition, while the OFA group showed no such effect. There was no effect on horizontal saccade amplitudes. These combined results suggest that OPA might serve to represent local scene information that can then be utilized by visuomotor control networks to guide gaze allocation in natural scenes. |
James Mathew; Frederic R. Danion Ups and downs in catch-up saccades following single-pulse TMS-methodological considerations Journal Article In: PLoS ONE, vol. 13, no. 10, pp. e0205208, 2018. @article{Mathew2018a, Transcranial magnetic stimulation (TMS) can interfere with smooth pursuit or with saccades initiated from a fixed position toward a fixed target, but little is known about the effect of TMS on catch-up saccade made to assist smooth pursuit. Here we explored the effect of TMS on catch-up saccades by means of a situation in which the moving target was driven by an external agent, or moved by the participants' hand, a condition known to decrease the occurrence of catch-up saccade. Two sites of stimulation were tested, the vertex and M1 hand area. Compared to conditions with no TMS, we found a consistent modulation of saccadic activity after TMS such that it decreased at 40-100ms, strongly resumed at 100-160ms, and then decreased at 200-300ms. Despite this modulatory effect, the accuracy of catch-up saccade was maintained, and the mean saccadic activity over the 0-300ms period remained unchanged. Those findings are discussed in the context of studies showing that single-pulse TMS can induce widespread effects on neural oscillations as well as perturbations in the latency of saccades during reaction time protocols. At a more general level, despite challenges and interpretational limitations making uncertain the origin of this modulatory effect, our study provides direct evidence that TMS over presumably non-oculomotor regions interferes with the initiation of catch-up saccades, and thus offers methodological considerations for future studies that wish to investigate the underlying neural circuitry of catch-up saccades using TMS. |
Denis Pélisson; Ouazna Habchi; Muriel T. N. Panouillères; Charles Hernoux; Alessandro Farnè A cortical substrate for the long-term memory of saccadic eye movements calibration Journal Article In: NeuroImage, vol. 179, pp. 348–356, 2018. @article{Pelisson2018, How movements are continuously adapted to physiological and environmental changes is a fundamental question in systems neuroscience. While many studies have elucidated the mechanisms which underlie short-term sensorimotor adaptation (∼10–30 min), how these motor memories are maintained over longer-term (>3–5 days) -and thanks to which neural systems-is virtually unknown. Here, we examine in healthy human participants whether the temporo-parietal junction (TPJ) is causally involved in the induction and/or the retention of saccadic eye movements' adaptation. Single-pulse transcranial magnetic stimulation (spTMS) was applied while subjects performed a ∼15min size-decrease adaptation task of leftward reactive saccades. A TMS pulse was delivered over the TPJ in the right hemisphere (rTPJ) in each trial either 30, 60, 90 or 120 msec (in 4 separate adaptation sessions) after the saccade onset. In two control groups of subjects, the same adaptation procedure was achieved either alone (No-TMS) or combined with spTMS applied over the vertex (SHAM-TMS). While the timing of spTMS over the rTPJ did not significantly affect the speed and immediate after-effect of adaptation, we found that the amount of adaptation retention measured 10 days later was markedly larger (42%) than in both the No-TMS (21%) and the SHAM-TMS (11%) control groups. These results demonstrate for the first time that the cerebral cortex is causally involved in maintaining long-term oculomotor memories. |
2017 |
Daniel J. Acheson; Peter Hagoort Stimulating the brainʼs language network: Syntactic ambiguity resolution after TMS to the inferior frontal gyrus and middle temporal gyrus Journal Article In: Journal of Cognitive Neuroscience, vol. 25, no. 10, pp. 1664–1677, 2017. @article{Acheson2017, The posterior middle temporal gyrus (MTG) and inferior frontal gyrus (IFG) are two critical nodes of the brainʼs language network. Previous neuroimaging evidence has supported a dis- sociation in language comprehension in which parts of the MTG are involved in the retrieval of lexical syntactic informa- tion and the IFG in unification operations that maintain, select, and integrate multiple sources of information over time. In the present investigation, we tested for causal evidence of this dis- sociation by modulating activity in IFG and MTG using an off- line TMS procedure: continuous theta-burst stimulation. Lexical–syntactic retrieval was manipulated by using sentences with and without a temporarily word-class (noun/verb) ambiguity (e.g., run). In one group of participants, TMS was applied to the IFG and MTG, and in a control group, no TMS was applied. Eye movements were recorded and quantified at two critical sentence regions: a temporarily ambiguous region and a disambig- uating region. Results show that stimulation of the IFG led to a modulation of the ambiguity effect (ambiguous–unambiguous) at the disambiguating sentence region in three measures: first fixation durations, total reading times, and regressive eye movements into the region. Both IFG and MTG stimulation modulated the ambiguity effect for total reading times in the temporarily ambiguous sentence region relative to the control group. The current results demonstrate that an offline repetitive TMS protocol can have influences at a different point in time during online processing and provide causal evidence for IFG involvement in unification operations during sentence comprehension. |
Hui-Yan Chiau; Neil G. Muggleton; Chi-Hung Juan Exploring the contributions of the supplementary eye field to subliminal inhibition using double-pulse transcranial magnetic stimulation Journal Article In: Human Brain Mapping, vol. 38, pp. 339–351, 2017. @article{Chiau2017, It is widely accepted that the supplementary eye fields (SEF) are involved in the control of voluntary eye movements. However, recent evidence suggests that SEF may also be important for unconscious and involuntary motor processes. Indeed, Sumner et al. ([2007]: Neuron 54:697-711) showed that patients with micro-lesions of the SEF demonstrated an absence of subliminal inhibition as evoked by masked-prime stimuli. Here, we used double-pulse transcranial magnetic stimulation (TMS) in healthy volunteers to investigate the role of SEF in subliminal priming. We applied double-pulse TMS at two time windows in a masked-prime task: the first during an early phase, 20-70 ms after the onset of the mask but before target presentation, during which subliminal inhibition is present; and the second during a late phase, 20-70 ms after target onset, during which the saccade is being prepared. We found no effect of TMS with the early time window of stimulation, whereas a reduction in the benefit of an incompatible subliminal prime stimulus was found when SEF TMS was applied at the late time window. These findings suggest that there is a role for SEF related to the effects of subliminal primes on eye movements, but the results do not support a role in inhibiting the primed tendency. |
Sergio Delle Monache; Francesco Lacquaniti; Gianfranco Bosco In: Journal of Neurophysiology, vol. 118, no. 3, pp. 1809–1823, 2017. @article{DelleMonache2017, The ability to catch objects when tran- siently occluded from view suggests their motion can be extrapolated. Intraparietal cortex (IPS) plays a major role in this process along with other brain structures, depending on the task. For example, intercep- tion of objects under Earth's gravity effects may depend on time-to-contact predictions derived from integration of visual signals processed by hMT/V5⫹ with a priori knowledge of gravity residing in the temporoparietal junction (TPJ). To investigate this issue further, we disrupted TPJ, hMT/V5⫹, and IPS activities with transcranial magnetic stimulation (TMS) while subjects intercepted computer- simulated projectile trajectories perturbed randomly with either hypo- or hypergravity effects. In experiment 1, trajectories were occluded either 750 or 1,250 ms before landing. Three subject groups underwent triple-pulse TMS (tpTMS, 3 pulses at 10 Hz) on one target area (TPJ | hMT/V5⫹ | IPS) and on the vertex (control site), timed at either trajectory perturbation or occlusion. In experiment 2, trajectories were entirely visible and participants received tpTMS on TPJ and hMT/ V5+ with same timing as experiment 1. tpTMS of TPJ, hMT/V5⫹, and IPS affected differently the interceptive timing. TPJ stimulation affected preferentially responses to 1-g motion, hMT/V5+ all response types, and IPS stimulation induced opposite effects on 0-g and 2-g responses, being ineffective on 1-g responses. Only IPS stimulation was effective when applied after target disappearance, implying this area might elaborate memory representations of occluded target motion. Results are compatible with the idea that IPS, TPJ, and hMT/V5+ contribute to distinct aspects of visual motion extrapolation, perhaps through parallel processing. |
Grace Edwards; Céline Paeye; Philippe Marque; Rufin VanRullen; Patrick Cavanagh Predictive position computations mediated by parietal areas: TMS evidence Journal Article In: NeuroImage, vol. 153, pp. 49–57, 2017. @article{Edwards2017, When objects move or the eyes move, the visual system can predict the consequence and generate a percept of the target at its new position. This predictive localization may depend on eye movement control in the frontal eye fields (FEF) and the intraparietal sulcus (IPS) and on motion analysis in the medial temporal area (MT). Across two experiments we examined whether repetitive transcranial magnetic stimulation (rTMS) over right FEF, right IPS, right MT, and a control site, peripheral V1/V2, diminished participants' perception of two cases of predictive position perception: trans-saccadic fusion, and the flash grab illusion, both presented in the contralateral visual field. In trans-saccadic fusion trials, participants saccade toward a stimulus that is replaced with another stimulus during the saccade. Frequently, predictive position mechanisms lead to a fused percept of pre- and post-saccade stimuli (Paeye et al., 2017). We found that rTMS to IPS significantly decreased the frequency of perceiving trans-saccadic fusion within the first 10 min after stimulation. In the flash grab illusion, a target is flashed on a moving background leading to the percept that the target has shifted in the direction of the motion after the flash (Cavanagh and Anstis, 2013). In the first experiment, the reduction in the flash grab illusion after rTMS to IPS and FEF did not reach significance. In the second experiment, using a stronger version of the flash grab, the illusory shift did decrease significantly after rTMS to IPS although not after rTMS to FEF or to MT. These findings suggest that right IPS contributes to predictive position perception during saccades and motion processing in the contralateral visual field. |
Wayne E. MacKey; Clayton E. Curtis Distinct contributions by frontal and parietal cortices support working memory Journal Article In: Scientific Reports, vol. 7, pp. 6188, 2017. @article{MacKey2017, Although subregions of frontal and parietal cortex both contribute and coordinate to support working memory (WM) functions, their distinct contributions remain elusive. Here, we demonstrate that perturbations to topographically organized human frontal and parietal cortex during WM maintenance cause distinct but systematic distortions in WM. The nature of these distortions supports theories positing that parietal cortex mainly codes for retrospective sensory information, while frontal cortex codes for prospective action. |
James Mathew; Alexandre Eusebio; Frederic R. Danion Limited contribution of primary motor cortex in eye-hand coordination: A TMS study Journal Article In: Journal of Neuroscience, vol. 37, no. 40, pp. 9730 –9740, 2017. @article{Mathew2017, The ability to track a moving target with the eye is substantially improved when the target is self-moved compared with when it is moved by an external agent. To account for this observation, it has been postulated that the oculomotor system has access to hand efference copy, thereby allowing to predict the motion of the visual target. Along this scheme, we tested the effect of transcranial magnetic stimulation (TMS) over the hand area of the primary motor cortex (M1) when human participants (50% females) are asked to track with their eyes a visual target whose horizontal motion is driven by their grip force. We reasoned that, if the output of M1 is used by the oculomotor system to keep track of the target, on top of inducing short latency disturbance of grip force, single-pulse TMS should also quickly disrupt ongoing eye motion. For comparison purposes, the effect of TMS over M1 was monitored when subjects tracked an externally moved target (while keeping their hand at rest or not). In both cases, results showed no alterations in smooth pursuit, meaning that its velocity was unaffected within the 25-125 ms epoch that followed TMS. Overall, our results imply that the output of M1 has limited contribution in driving the eye motion during our eye-hand coordination task. This study suggests that, if hand motor signals are accessed by the oculomotor system, this is upstream of M1. |
Rebecca E. Paladini; René M. Müri; Jurka Meichtry; Tobias Nef; Fred W. Mast; Urs P. Mosimann; Thomas Nyffeler; Dario Cazzoli The influence of alertness on the spatial deployment of visual attention is mediated by the excitability of the posterior parietal cortices Journal Article In: Cerebral Cortex, vol. 27, no. 1, pp. 233–243, 2017. @article{Paladini2017, With a reduced level of alertness, healthy individuals typically show a rightward shift when deploying visual attention in space. The impact of alertness on the neural networks governing visuospatial attention is, however, poorly understood. By using a transcranial magnetic stimulation twin-coil approach, the present study aimed at investigating the effects of an alertness manipulation on the excitability of the left and the right posterior parietal cortices (PPCs), crucial nodes of the visuospatial attentional network. Participants' visuospatial attentional deployment was assessed with a free visual exploration task and concurrent eye tracking. Their alertness level was manipulated through the time of the day, that is, by testing chronotypically defined evening types both during their circadian on- and off-peak times. The results revealed an increased excitability of the left compared with the right PPC during low alertness. On the horizontal dimension, these results were accompanied by a significant rightward shift in the center and a bilateral narrowing in the periphery of the visual exploration field, as well as a central upward shift on the vertical dimension. The findings show that the manipulation of non-spatial attentional aspects (i.e., alertness) can affect visuospatial attentional deployment and modulate the excitability of areas subtending spatial attentional control. |
2016 |
Melanie R. Burke; R. O. Coats Dissociation of the rostral and dorsolateral prefrontal cortex during sequence learning in saccades: A TMS investigation Journal Article In: Experimental Brain Research, vol. 234, no. 2, pp. 597–604, 2016. @article{Burke2016, This experiment sought to find whether differences exist between the dorsolateral prefrontal cortex (DLPFC) and the medial rostral prefrontal cortex (MRPFC) for performing stimulus-independent and stimulus-oriented tasks, respectively. To find a causal relationship in these areas, we employed the use of trans-cranial magnetic stimulation (TMS). Prefrontal areas were stimulated whilst participants performed random or predictable sequence learning tasks at stimulus onset (1st presentation of the sequence only for both Random and Predictable), or during the inter-sequence interval. Overall, we found that during the predictable task a significant decrease in saccade latency, gain and duration was found when compared to the randomised conditions, as expected and observed previously. However, TMS stimulation in DLPFC during the delay in the predictive sequence learning task reduced this predictive ability by delaying the saccadic onset and generating abnormal reductions in saccadic gains during prediction. In contrast, we found that stimulation during a delay in MRPFC reversed the normal effects on peak velocity of the task with the predictive task revealing higher peak velocity than the randomised task. These findings provide causal evidence for independent functions of DLPFC and MRPFC in performing stimulus-independent processing during sequence learning in saccades. |
Sarah C. Krall; Lukas J. Volz; Eileen Oberwelland; Christian Grefkes; Gereon R. Fink; Kerstin Konrad The right temporoparietal junction in attention and social interaction: A transcranial magnetic stimulation study Journal Article In: Human Brain Mapping, vol. 37, no. 2, pp. 796–807, 2016. @article{Krall2016, The right temporoparietal junction (rTPJ) has been associated with the ability to reorient attention to unexpected stimuli and the capacity to understand others' mental states (theory of mind [ToM]/false belief). Using activation likelihood estimation meta-analysis we previously unraveled that the anterior rTPJ is involved in both, reorienting of attention and ToM, possibly indicating a more general role in attention shifting. Here, we used neuronavigated transcranial magnetic stimulation to directly probe the role of the rTPJ across attentional reorienting and false belief. Task performance in a visual cueing paradigm and false belief cartoon task was investigated after application of continuous theta burst stimulation (cTBS) over anterior rTPJ (versus vertex, for control). We found that attentional reorienting was significantly impaired after rTPJ cTBS compared with control. For the false belief task, error rates in trials demanding a shift in mental state significantly increased. Of note, a significant positive correlation indicated a close relation between the stimulation effect on attentional reorienting and false belief trials. Our findings extend previous neuroimaging evidence by indicating an essential overarching role of the anterior rTPJ for both cognitive functions, reorienting of attention and ToM. |
Romain Quentin; Seth E. Frankston; Marine Vernet; Monica N. Toba; Paolo Bartolomeo; Lorena Chanes; Antoni Valero-Cabré In: Cerebral Cortex, vol. 26, no. 6, pp. 2381–2390, 2016. @article{Quentin2016, Behavioral and electrophysiological studies in humans and non-human primates have correlated frontal high-beta activity with the orienting of endogenous attention and shown the ability of the latter function to modulate visual performance. We here combined rhythmic transcranial magnetic stimulation (TMS) and diffusion imaging to study the relation between frontal oscillatory activity and visual performance, and we associated these phenomena to a specific set of white matter pathways that in humans subtend attentional processes. High-beta rhythmic activity on the right frontal eye field (FEF) was induced with TMS and its causal effects on a contrast sensitivity function were recorded to explore its ability to improve visual detection performance across different stimulus contrast levels. Our results show that frequency-specific activity patterns engaged in the right FEF have the ability to induce a leftward shift of the psychometric function. This increase in visual performance across different levels of stimulus contrast is likely mediated by a contrast gain mechanism. Interestingly, microstructural measures of white matter connectivity suggest a strong implication of right fronto-parietal connectivity linking the FEF and the intraparietal sulcus in propagating high-beta rhythmic signals across brain networks and subtending top-down frontal influences on visual performance. |
Hongfang Wang; Eleanor Callaghan; Gerard Gooding-Williams; Craig McAllister; Klaus Kessler Rhythm makes the world go round: An MEG-TMS study on the role of right TPJ theta oscillations in embodied perspective taking Journal Article In: Cortex, vol. 75, pp. 68–81, 2016. @article{Wang2016e, While some aspects of social processing are shared between humans and other species, some aspects are not. The former seems to apply to merely tracking another's visual perspective in the world (i.e., what a conspecific can or cannot perceive), while the latter applies to perspective taking in form of mentally "embodying" another's viewpoint. Our previous behavioural research had indicated that only perspective taking, but not tracking, relies on simulating a body schema rotation into another's viewpoint. In the current study we employed Magnetoencephalography (MEG) and revealed that this mechanism of mental body schema rotation is primarily linked to theta oscillations in a wider brain network of body-schema, somatosensory and motor-related areas, with the right posterior temporo-parietal junction (pTPJ) at its core. The latter was reflected by a convergence of theta oscillatory power in right pTPJ obtained by overlapping the separately localised effects of rotation demands (angular disparity effect), cognitive embodiment (posture congruence effect), and basic body schema involvement (posture relevance effect) during perspective taking in contrast to perspective tracking. In a subsequent experiment we interfered with right pTPJ processing using dual pulse Transcranial Magnetic Stimulation (dpTMS) and observed a significant reduction of embodied processing. We conclude that right TPJ is the crucial network hub for transforming the embodied self into another's viewpoint, body and/or mind, thus, substantiating how conflicting representations between self and other may be resolved and potentially highlighting the embodied origins of high-level social cognition in general. |
2015 |
Jamila Andoh; Reiko Matsushita; Robert J. Zatorre Asymmetric interhemispheric transfer in the auditory network: Evidence from TMS, resting-state fMRI, and diffusion imaging Journal Article In: Journal of Neuroscience, vol. 43, no. 43, pp. 14602–14611, 2015. @article{Andoh2015, Hemispheric asymmetries in human auditory cortical function and structure are still highly debated. Brain stimulation approaches can complement correlational techniques by uncovering causal influences. Previous studies have shown asymmetrical effects of transcranial magnetic stimulation (TMS) on task performance, but it is unclear whether these effects are task-specific or reflect intrinsic network properties. To test how modulation of auditory cortex (AC) influences functional networks and whether this influence is asymmetrical, the present study measured resting-state fMRI connectivity networks in 17 healthy volunteers before and immediately after TMS (continuous theta burst stimulation) to the left or right AC, and the vertex as a control. We also examined the relationship between TMS-induced interhemispheric signal propagation and anatomical properties of callosal auditory fibers as measured with diffusion-weighted MRI. We found that TMS to the right AC, but not the left, resulted in widespread connectivity decreases in auditory- and motor-related networks in the resting state. Individual differences in the degree of change in functional connectivity between auditory cortices after TMS applied over the right AC were negatively related to the volume of callosal auditory fibers. The findings show that TMS-induced network modulation occurs, even in the absence of an explicit task, and that the magnitude of the effect differs across individuals as a function of callosal structure, supporting a role for the corpus callosum in mediating functional asymmetry. The findings support theoretical models emphasizing hemispheric differences in network organization and are of practical significance in showing that brain stimulation studies need to take network-level effects into account. |
Dario Cazzoli; René M. Müri; Christopher Kennard; Clive R. Rosenthal The role of the right posterior parietal cortex in letter migration between words Journal Article In: Journal of Cognitive Neuroscience, vol. 27, no. 2, pp. 377–386, 2015. @article{Cazzoli2015a, When briefly presented with pairs of words, skilled readers can sometimes report words with migrated letters (e.g., they report hunt when presented with the words hint and hurt). This and other letter migration phenomena have been often used to investigate factors that influence reading such as letter position coding. However, the neural basis of letter migration is poorly understood. Previous evidence has implicated the right posterior parietal cortex (PPC) in processing visuospatial attributes and lexical properties during word reading. The aim of this study was to assess this putative role by combining an inhibitory TMS protocol with a letter migration paradigm, which was designed to examine the contributions of visuospatial attributes and lexical factors. Temporary interference with the right PPC led to three specific effects on letter migration. First, the number of letter migrations was significantly increased only in the group with active stimulation (vs. a sham stimulation group or a control group without stimulation), and there was no significant effect on other error types. Second, this effect occurred only when letter migration could result in a meaningful word (migration vs. control context). Third, the effect of active stimulation on the number of letter migrations was lateralized to target words presented on the left. Our study thus demonstrates that the right PPC plays a specific and causal role in the phenomenon of letter migration. The nature of this role cannot be explained solely in terms of visuospatial attention, rather it involves an interplay between visuospatial attentional and word reading-specific factors. |
Magdalena Chechlacz; Glyn W. Humphreys; Stamatios N. Sotiropoulos; Christopher Kennard; Dario Cazzoli Structural organization of the corpus callosum predicts attentional shifts after continuous theta burst stimulation Journal Article In: Journal of Neuroscience, vol. 35, no. 46, pp. 15353–15368, 2015. @article{Chechlacz2015, Repetitive transcranial magnetic stimulation (rTMS) applied over the right posterior parietal cortex (PPC) in healthy participants has been shown to trigger a significant rightward shift in the spatial allocation of visual attention, temporarily mimicking spatial deficits observed in neglect. In contrast, rTMS applied over the left PPC triggers a weaker or null attentional shift. However, large interindividual differences in responses to rTMS have been reported. Studies measuring changes in brain activation suggest that the effects of rTMS may depend on both interhemispheric and intrahemispheric interactions between cortical loci controlling visual attention. Here, we investigated whether variability in the structural organization of human white matter pathways subserving visual attention, as assessed by diffusion magnetic resonance imaging and tractography, could explain interindividual differences in the effects of rTMS. Most participants showed a rightward shift in the allocation of spatial attention after rTMS over the right intraparietal sulcus (IPS), but the size of this effect varied largely across participants. Conversely, rTMS over the left IPS resulted in strikingly opposed individual responses, with some participants responding with rightward and some with leftward attentional shifts. We demonstrate that microstructural and macrostructural variability within the corpus callosum, consistent with differential effects on cross-hemispheric interactions, predicts both the extent and the direction of the response to rTMS. Together, our findings suggest that the corpus callosum may have a dual inhibitory and excitatory function in maintaining the interhemispheric dynamics that underlie the allocation of spatial attention. |
Tom A. Graaf; Felix Duecker; Martin H. P. Fernholz; Alexander T. Sack Spatially specific vs. unspecific disruption of visual orientation perception using chronometric pre-stimulus TMS Journal Article In: Frontiers in Behavioral Neuroscience, vol. 9, pp. 5, 2015. @article{Graaf2015, Transcranial magnetic stimulation (TMS) over occipital cortex can impair visual processing. Such ‘TMS masking' has repeatedly been shown at several stimulus onset asynchronies (SOAs), with TMS pulses generally applied after the onset of a visual stimulus. Following increased interest in the neuronal state-dependency of visual processing, we recently explored the efficacy of TMS at ‘negative SOAs', when no visual processing can yet occur. We could reveal pre-stimulus TMS disruption, with results moreover hinting at two separate mechanisms in occipital cortex biasing subsequent orientation perception. Here we extended this work, including a chronometric design to map the temporal dynamics of spatially specific and unspecific mechanisms of state-dependent visual processing, while moreover controlling for TMS-induced pupil covering. TMS pulses applied 60-40 ms prior to a visual stimulus decreased orientation processing independent of stimulus location, while a local suppressive effect was found for TMS applied 30-10 ms pre-stimulus. These results contribute to our understanding of spatiotemporal mechanisms in occipital cortex underlying the state-dependency of visual processing, providing a basis for future work to link pre-stimulus TMS suppression effects to other known visual biasing mechanisms. |
Peter H. Donaldson; Caroline T. Gurvich; Joanne Fielding; Peter G. Enticott Exploring associations between gaze patterns and putative human mirror neuron system activity Journal Article In: Frontiers in Human Neuroscience, vol. 9, pp. 523, 2015. @article{Donaldson2015, The human mirror neuron system (MNS) is hypothesized to be crucial to social cognition. Given that key MNS-input regions such as the superior temporal sulcus are involved in biological motion processing, and mirror neuron activity in monkeys has been shown to vary with visual attention, aberrant MNS function may be partly attributable to atypical visual input. To examine the relationship between gaze pattern and interpersonal motor resonance (IMR; an index of putative MNS activity), healthy right-handed participants aged 18–40 (n = 26) viewed videos of transitive grasping actions or static hands, whilst the left primary motor cortex received transcranial magnetic stimulation. Motor- evoked potentials recorded in contralateral hand muscles were used to determine IMR. Participants also underwent eyetracking analysis to assess gaze patterns whilst viewing the same videos. No relationship was observed between predictive gaze and IMR. However, IMR was positively associated with fixation counts in areas of biological motion in the videos, and negatively associated with object areas. These findings are discussed with reference to visual influences on the MNS, and the possibility that MNS atypicalities might be influenced by visual processes such as aberrant gaze pattern. |
Pankhuri Malik; Joost C. Dessing; J. Douglas Crawford Role of early visual cortex in trans-saccadic memory of object features Journal Article In: Journal of Vision, vol. 15, no. 7, pp. 1–17, 2015. @article{Malik2015, Early visual cortex (EVC) participates in visual feature memory and the updating of remembered locations across saccades, but its role in the trans-saccadic integration of object features is unknown. We hypothesized that if EVC is involved in updating object features relative to gaze, feature memory should be disrupted when saccades remap an object representation into a simultaneously perturbed EVC site. To test this, we applied transcranial magnetic stimulation (TMS) over functional magnetic resonance imaging–localized EVC clusters corresponding to the bottom left/right visual quadrants (VQs). During experiments, these VQs were probed psychophysically by briefly presenting a central object (Gabor patch) while subjects fixated gaze to the right or left (and above). After a short memory interval, participants were required to detect the relative change in orientation of a re-presented test object at the same spatial location. Participants either sustained fixation during the memory interval (fixation task)ormade a horizontal saccade that either maintained or reversed the VQ of the object (saccade task). Three TMS pulses (coinciding with the pre-, peri-, and postsaccade intervals) were applied to the left or right EVC. This had no effect when (a) fixation was maintained, (b) saccades kept the object in the same VQ, or (c) the EVC quadrant corresponding to the first object was stimulated. However, as predicted, TMS reduced performance when saccades (especially larger saccades) crossed the remembered object location and brought it into the VQ corresponding to the TMS site. This suppression effect was statistically significant for leftward saccades and followed a weaker trend for rightward saccades. These causal results are consistent with the idea that EVC is involved in the gaze-centered updating of object features for trans-saccadic memory and perception. |
Tom R. Marshall; Til Ole Bergmann; Ole Jensen Frontoparietal structural connectivity mediates the top-down control of neuronal synchronization associated with selective attention Journal Article In: PLoS Biology, vol. 13, no. 10, pp. e1002272, 2015. @article{Marshall2015, Neuronal synchronization reflected by oscillatory brain activity has been strongly implicated in the mechanisms supporting selective gating. We here aimed at identifying the anatomical pathways in humans supporting the top-down control of neuronal synchronization. We first collected diffusion imaging data using magnetic resonance imaging to identify the medial branch of the superior longitudinal fasciculus (SLF), a white-matter tract connecting frontal control areas to parietal regions. We then quantified the modulations in oscillatory activity using magnetoencephalography in the same subjects performing a spatial attention task. We found that subjects with a stronger SLF volume in the right compared to the left hemi- sphere (or vice versa) also were the subjects who had a better ability to modulate right com- pared to left hemisphere alpha and gamma band synchronization, with the latter also predicting biases in reaction time. Our findings implicate the medial branch of the SLF in mediating top-down control of neuronal synchronization in sensory regions that support selective attention. |
Petra Vetter; Marie-Hélène Grosbras; Lars Muckli TMS over V5 disrupts motion prediction Journal Article In: Cerebral Cortex, vol. 25, no. 4, pp. 1052–1059, 2015. @article{Vetter2015, Given the vast amount of sensory information the brain has to deal with, predicting some of this information based on the current context is a resource-efficient strategy. The framework of predictive coding states that higher-level brain areas generate a predictive model to be communicated via feedback connections to early sensory areas. Here, we directly tested the necessity of a higher-level visual area, V5, in this predictive processing in the context of an apparent motion paradigm. We flashed targets on the apparent motion trace in-time or out-of-time with the predicted illusory motion token. As in previous studies, we found that predictable in-time targets were better detected than unpredictable out-of-time targets. However, when we applied functional magnetic resonance imaging-guided, double-pulse transcranial magnetic stimulation (TMS) over left V5 at 13-53 ms before target onset, the detection advantage of in-time targets was eliminated; this was not the case when TMS was applied over the vertex. Our results are causal evidence that V5 is necessary for a prediction effect, which has been shown to modulate V1 activity (Alink et al. 2010). Thus, our findings suggest that information processing between V5 and V1 is crucial for visual motion prediction, providing experimental support for the predictive coding framework. |
Alexandre Zenon; Mariam Sidibe; Etienne Olivier Disrupting the supplementary motor area makes physical effort appear less effortful Journal Article In: Journal of Neuroscience, vol. 35, no. 23, pp. 8737–8744, 2015. @article{Zenon2015, The perception of physical effort is relatively unaffected by the suppression of sensory afferences, indicating that this function relies mostly on the processing of the central motor command. Neural signals in the supplementary motor area (SMA) correlate with the intensity of effort, suggesting that the motor signal involved in effort perception could originate from this area, but experimental evidence supporting this view is still lacking. Here, we tested this hypothesis by disrupting neural activity in SMA, in primary motor cortex (M1), or in a control site by means of continuous theta-burst transcranial magnetic stimulation, while measuring effort perception during grip forces of different intensities. After each grip force exertion, participants had the opportunity to either accept or refuse to replicate the same effort for varying amounts of reward. In addition to the subjective rating of perceived exertion, effort perception was estimated on the basis of the acceptance rate, the effort replication accuracy, the influence of the effort exerted in trial t on trial t+1, and pupil dilation. We found that disruption of SMA activity, but not of M1, led to a consistent decrease in effort perception, whatever the measure used to assess it. Accordingly, we modeled effort perception in a structural equation model and found that only SMA disruption led to a significant alteration of effort perception. These findings indicate that effort perception relies on the processing of a signal originating from motor-related neural circuits upstream of M1 and that SMA is a key node of this network. |
2014 |
Lysianne Beynel; Alan Chauvin; Nathalie Guyader; Sylvain Harquel; Thierry Bougerol; Christian Marendaz; David Szekely What saccadic eye movements tell us about TMS-induced neuromodulation of the DLPFC and mood changes: A pilot study in bipolar disorders Journal Article In: Frontiers in Integrative Neuroscience, vol. 8, pp. 65, 2014. @article{Beynel2014, The study assumed that the antisaccade (AS) task is a relevant psychophysical tool to assess (i) short-term neuromodulation of the dorsolateral prefrontal cortex (DLPFC) induced by intermittent theta burst stimulation (iTBS); and (ii) mood change occurring during the course of the treatment. Saccadic inhibition is known to strongly involve the DLPFC, whose neuromodulation with iTBS requires less stimulation time and lower stimulation intensity, as well as results in longer aftereffects than the conventional repetitive transcranial magnetic stimulation (rTMS). Active or sham iTBS was applied every day for 3 weeks over the left DLPFC of 12 drug-resistant bipolar depressed patients. To assess the iTBS-induced short-term neuromodulation, the saccadic task was performed just before (S1) and just after (S2) the iTBS session, the first day of each week. Mood was evaluated through Montgomery and Asberg Depression Rating Scale (MADRS) scores and the difference in scores between the beginning and the end of treatment was correlated with AS performance change between these two periods. As expected, only patients from the active group improved their performance from S1 to S2 and mood improvement was significantly correlated with AS performance improvement. In addition, the AS task also discriminated depressive bipolar patients from healthy control subjects. Therefore, the AS task could be a relevant and useful tool for clinicians to assess if the Transcranial magnetic stimulation (TMS)-induced short-term neuromodulation of the DLPFC occurs as well as a “trait vs. state” objective marker of depressive mood disorder. |
Marc R. Kamke; Alexander E. Ryan; Martin V. Sale; Megan E. J. Campbell; Stephan Riek; Timothy J. Carroll; Jason B. Mattingley Visual spatial attention has opposite effects on bidirectional plasticity in the human motor cortex Journal Article In: Journal of Neuroscience, vol. 34, no. 4, pp. 1475–1480, 2014. @article{Kamke2014, Long-term potentiation (LTP) and long-term depression (LTD) are key mechanisms of synaptic plasticity that are thought to act in concert to shape neural connections. Here we investigated the influence of visual spatial attention on LTP-like and LTD-like plasticity in the human motor cortex. Plasticity was induced using paired associative stimulation (PAS), which involves repeated pairing of peripheral nerve stimulation and transcranial magnetic stimulation to alter functional responses in the thumb area of the primary motor cortex. PAS-induced changes in cortical excitability were assessed using motor-evoked potentials. During plasticity induction, participants directed their attention to one of two visual stimulus streams located adjacent to each hand. When participants attended to visual stimuli located near the left thumb, which was targeted by PAS, LTP-like increases in excitability were significantly enhanced, and LTD-like decreases in excitability reduced, relative to when they attended instead to stimuli located near the right thumb. These differential effects on (bidirectional) LTP-like and LTD-like plasticity suggest that voluntary visual attention can exert an important influence on the functional organization of the motor cortex. Specifically, attention acts to both enhance the strengthening and suppress the weakening of neural connections representing events that fall within the focus of attention. |
Kohitij Kar; Bart Krekelberg Transcranial alternating current stimulation attenuates visual motion adaptation Journal Article In: Journal of Neuroscience, vol. 34, no. 21, pp. 7334–7340, 2014. @article{Kar2014, Transcranial alternating current stimulation (tACS) is used in clinical applications and basic neuroscience research. Although its behavioral effects are evident from prior reports, current understanding of the mechanisms that underlie these effects is limited. We used motion perception, a percept with relatively well known properties and underlying neural mechanisms to investigate tACS mechanisms. Healthy human volunteers showed a surprising improvement in motion sensitivity when visual stimuli were paired with 10 Hz tACS. In addition, tACS reduced the motion-after effect, and this reduction was correlated with the improvement in motion sensitivity. Electrical stimulation had no consistent effect when applied before presenting a visual stimulus or during recovery from motion adaptation. Together, these findings suggest that perceptual effects of tACS result from an attenuation of adaptation. Important consequences for the practical use of tACS follow from our work. First, because this mechanism interferes only with adaptation, this suggests that tACS can be targeted at subsets of neurons (by adapting them), even when the applied currents spread widely throughout the brain. Second, by interfering with adaptation, this mechanism provides a means by which electrical stimulation can generate behavioral effects that outlast the stimulation. |
Benjamin D. Lester; Paul Dassonville The role of the right superior parietal lobule in processing visual context for the establishment of the egocentric reference frame Journal Article In: Journal of Cognitive Neuroscience, vol. 26, no. 10, pp. 2201–2209, 2014. @article{Lester2014, Visual cues contribute to the creation of an observerʼs ego- centric reference frame, within which the locations and orien- tations of objects can be judged. However, these cues can also be misleading. In the rod-and-frame illusion, for example, a large tilted frame distorts the observerʼs sense of vertical, caus- ing an enclosed rod to appear tilted in the opposite direction. To determine the brain region responsible for processing these spatial cues, we used TMS to suppress neural activity in the superior parietal lobule of healthy observers. Stimulation of the right hemisphere, but not the left, caused a significant reduc- tion in rod-and-frame susceptibility. In contrast, a tilt illusion caused by a mechanism that does not involve a distortion of the observerʼs egocentric reference frame was unaffected. These results demonstrate that the right superior parietal lobule is actively involved in processing the contextual cues that contribute to our perception of egocentric space. |
Indra T. Mahayana; Chia-Lun Liu; Chi Fu Chang; Daisy L. Hung; Ovid J. L. Tzeng; Chi-Hung Juan; Neil G. Muggleton Far-space neglect in conjunction but not feature search following transcranial magnetic stimulation over right posterior parietal cortex Journal Article In: Journal of Neurophysiology, vol. 111, no. 4, pp. 705–714, 2014. @article{Mahayana2014, Near- and far-space coding in the human brain is a dynamic process. Areas in dorsal, as well as ventral visual association cortex, including right posterior parietal cortex (rPPC), right frontal eye field (rFEF), and right ventral occipital cortex (rVO), have been shown to be important in visuospatial processing, but the involvement of these areas when the information is in near or far space remains unclear. There is a need for investigations of these representations to help explain the pathophysiology of hemispatial neglect, and the role of near and far space is crucial to this. We used a conjunction visual search task using an elliptical array to investigate the effects of transcranial magnetic stimulation delivered over rFEF, rPPC, and rVO on the processing of targets in near and far space and at a range of horizontal eccentricities. As in previous studies, we found that rVO was involved in far-space search, and rFEF was involved regardless of the distance to the array. It was found that rPPC was involved in search only in far space, with a neglect-like effect when the target was located in the most eccentric locations. No effects were seen for any site for a feature search task. As the search arrays had higher predictability with respect to target location than is often the case, these data may form a basis for clarifying both the role of PPC in visual search and its contribution to neglect, as well as the importance of near and far space in these. |
Muriel T. N. Panouillères; Ouazna Habchi; Peggy Gerardin; Roméo Salemme; Christian Urquizar; Alessandro Farnè; Denis Pélisson A role for the parietal cortex in sensorimotor adaptation of saccades Journal Article In: Cerebral Cortex, vol. 24, no. 2, pp. 304–314, 2014. @article{Panouilleres2014, Sensorimotor adaptation ensures movement accuracy despite continuously changing environment and body. Adaptation of saccadic eye movements is a classical model of sensorimotor adaptation. Beside the well-established role of the brainstem-cerebellum in the adaptation of reactive saccades (RSs), the cerebral cortex has been suggested to be involved in the adaptation of voluntary saccades (VSs). Here, we provide direct evidence for a causal involvement of the parietal cortex in saccadic adaptation. First, the posterior intraparietal sulcus (pIPS) was identified in each subject using functional magnetic resonance imaging (fMRI). Then, a saccadic adaptation paradigm was used to progressively reduce the amplitude of RSs and VSs, while single-pulse transcranial magnetic stimulation (spTMS) was applied over the right pIPS. The perturbations of pIPS resulted in impairment for the adaptation of VSs, selectively when spTMS was applied 60 ms after saccade onset. In contrast, the adaptation of RSs was facilitated by spTMS applied 90 ms after saccade initiation. The differential effect of spTMS relative to saccade types suggests a direct interference with pIPS activity for the VS adaptation and a remote interference with brainstem-cerebellum activity for the RS adaptation. These results support the hypothesis that the adaptation of VSs and RSs involves different neuronal substrates. |
L. L. Tanaka; J. C. Dessing; Pankhuri Malik; S. L. Prime; J. Douglas Crawford The effects of TMS over dorsolateral prefrontal cortex on trans-saccadic memory of multiple objects Journal Article In: Neuropsychologia, vol. 63, pp. 185–193, 2014. @article{Tanaka2014, Humans typically make several rapid eye movements (saccades) per second. It is thought that visual working memory can retain and spatially integrate three to four objects or features across each saccade but little is known about this neural mechanism. Previously we showed that transcranial magnetic stimulation (TMS) to the posterior parietal cortex and frontal eye fields degrade trans-saccadic memory of multiple object features (Prime, Vesia, & Crawford, 2008, Journal of Neuroscience, 28(27), 6938-6949; Prime, Vesia, & Crawford, 2010, Cerebral Cortex, 20(4), 759-772.). Here, we used a similar protocol to investigate whether dorsolateral prefrontal cortex (DLPFC), an area involved in spatial working memory, is also involved in trans-saccadic memory. Subjects were required to report changes in stimulus orientation with (saccade task) or without (fixation task) an eye movement in the intervening memory interval. We applied single-pulse TMS to left and right DLPFC during the memory delay, timed at three intervals to arrive approximately 100. ms before, 100. ms after, or at saccade onset. In the fixation task, left DLPFC TMS produced inconsistent results, whereas right DLPFC TMS disrupted performance at all three intervals (significantly for presaccadic TMS). In contrast, in the saccade task, TMS consistently facilitated performance (significantly for left DLPFC/. perisaccadic TMS and right DLPFC/. postsaccadic TMS) suggesting a dis-inhibition of trans-saccadic processing. These results are consistent with a neural circuit of trans-saccadic memory that overlaps and interacts with, but is partially separate from the circuit for visual working memory during sustained fixation. |
Lin-Yuan Tseng; Philip Tseng; Wei-Kuang Liang; Daisy L. Hung; Ovid J. L. Tzeng; Neil G. Muggleton; Chi-Hung Juan The role of superior temporal sulcus in the control of irrelevant emotional face processing: A transcranial direct current stimulation study Journal Article In: Neuropsychologia, vol. 64, pp. 124–133, 2014. @article{Tseng2014a, Emotional faces are often salient cues of threats or other important contexts, and may therefore have a large effect on cognitive processes of the visual environment. Indeed, many behavioral studies have demonstrated that emotional information can modulate visual attention and eye movements. The aim of the present study was to investigate (1) how irrelevant emotional face distractors affect saccadic behaviors and (2) whether such emotional effects reflect a specific neural mechanism or merely biased selective attention. We combined a visual search paradigm that incorporated manipulation of different types of distractor (fearful faces or scrambled faces) and delivered anodal transcranial direct current stimulation (tDCS) over the superior temporal sulcus and the frontal eye field to investigate the functional roles of these areas in processing facial expressions and eye movements. Our behavioral data suggest that irrelevant emotional distractors can modulate saccadic behaviors. The tDCS results showed that while rFEF played a more general role in controlling saccadic behavior, rSTS is mainly involved in facial expression processing. Furthermore, rSTS played a critical role in processing facial expressions even when such expressions were not relevant to the task goal, implying that facial expressions and processing may be automatic irrespective of the task goal. |
Jessica M. Wright; Bart Krekelberg Transcranial direct current stimulation over posterior parietal cortex modulates visuospatial localization Journal Article In: Journal of Vision, vol. 14, no. 9, pp. 5–5, 2014. @article{Wright2014a, Visual localization is based on the complex interplay of bottom-up and top-down processing. Based on previous work, the posterior parietal cortex (PPC) is assumed to play an essential role in this interplay. In this study, we investigated the causal role of the PPC in visual localization. Specifically, our goal was to determine whether modulation of the PPC via transcranial direct current stimulation (tDCS) could induce visual mislocalization similar to that induced by an exogenous attentional cue (Wright, Morris, & Krekelberg, 2011). We placed one stimulation electrode over the right PPC and the other over the left PPC (dual tDCS) and varied the polarity of the stimulation. We found that this manipulation altered visual localization; this supports the causal involvement of the PPC in visual localization. Notably, mislocalization was more rightward when the cathode was placed over the right PPC than when the anode was placed over the right PPC. This mislocalization was found within a few minutes of stimulation onset, it dissipated during stimulation, but then resurfaced after stimulation offset and lasted for another 10-15 min. On the assumption that excitability is reduced beneath the cathode and increased beneath the anode, these findings support the view that each hemisphere biases processing to the contralateral hemifield and that the balance of activation between the hemispheres contributes to position perception (Kinsbourne, 1977; Szczepanski, Konen, & Kastner, 2010). |
2013 |
S. E. Bosch; Sebastiaan F. W. Neggers; Stefan Van der Stigchel The role of the frontal eye fields in oculomotor competition: Image-guided TMS enhances contralateral target selection Journal Article In: Cerebral Cortex, vol. 23, no. 4, pp. 824–832, 2013. @article{Bosch2013, In order to execute a correct eye movement to a target in a search display, a saccade program toward the target element must be activated, while saccade programs toward distracting elements must be inhibited. The aim of the present study was to elucidate the role of the frontal eye fields (FEFs) in oculomotor competition. Functional magnetic resonance imaging-guided single-pulse transcranial magnetic stimulation (TMS) was administered over either the left FEF, the right FEF, or the vertex (control site) at 3 time intervals after target presentation, while subjects performed an oculomotor capture task. When TMS was applied over the FEF contralateral to the visual field where a target was presented, there was less interference of an ipsilateral distractor compared with FEF stimulation ipsilateral to the target's visual field or TMS over vertex. Furthermore, TMS over the FEFs decreased latencies of saccades to the contralateral visual field, irrespective of whether the saccade was directed to the target or to the distractor. These findings show that single-pulse TMS over the FEFs enhances the selection of a target in the contralateral visual field and decreases saccade latencies to the contralateral visual field. |
Joost C. Dessing; Michael Vesia; J. Douglas Crawford The role of areas MT+/V5 and SPOC in spatial and temporal control of manual interception: An rTMS study Journal Article In: Frontiers in Behavioral Neuroscience, vol. 7, pp. 15, 2013. @article{Dessing2013, Manual interception, such as catching or hitting an approaching ball, requires the hand to contact a moving object at the right location and at the right time. Many studies have examined the neural mechanisms underlying the spatial aspects of goal-directed reaching, but the neural basis of the spatial and temporal aspects of manual interception are largely unknown. Here, we used repetitive transcranial magnetic stimulation (rTMS) to investigate the role of the human middle temporal visual motion area (MT+/V5) and superior parieto-occipital cortex (SPOC) in the spatial and temporal control of manual interception. Participants were required to reach-to-intercept a downward moving visual target that followed an unpredictably curved trajectory, presented on a screen in the vertical plane. We found that rTMS to MT+/V5 influenced interceptive timing and positioning, whereas rTMS to SPOC only tended to increase the spatial variance in reach end points for selected target trajectories. These findings are consistent with theories arguing that distinct neural mechanisms contribute to spatial, temporal, and spatiotemporal control of manual interception. |
Ada Le; Matthias Niemeier Left visual field preference for a bimanual grasping task with ecologically valid object sizes Journal Article In: Experimental Brain Research, vol. 230, pp. 187–196, 2013. @article{Le2013a, Grasping using two forelimbs in opposition to one another is evolutionary older than the hand with an opposable thumb (Whishaw and Coles in Behav Brain Res 77:135–148, 1996); yet, the mechanisms for bimanual grasps remain unclear. Similar to unimanual grasping, the localization of matching stable grasp points on an object is computationally expensive and so it makes sense for the signals to converge in a single cortical hemisphere. Indeed, bimanual grasps are faster and more accurate in the left visual field, and are disrupted if there is transcra- nial stimulation of the right hemisphere (Le and Niemeier in Exp Brain Res 224:263–273, 2013; Le et al. in Cereb Cortex. doi:10.1093/cercor/bht115, 2013). However, research so far has tested the right hemisphere dominance based on small objects only, which are usually grasped with one hand, whereas bimanual grasping is more com- monly used for objects that are too big for a single hand. Because grasping large objects might involve different neural circuits than grasping small objects (Grol et al. in J Neurosci 27:11877–11887, 2007), here we tested whether a left visual field/right hemisphere dominance for biman- ual grasping exists with large and thus more ecologically valid objects or whether the right hemisphere dominance is a function of object size. We asked participants to fixate to the left or right of an object and to grasp the object with the index and middle fingers of both hands. Consistent with previous observations, we found that for objects in the left visual field, the maximum grip apertures were scaled closer to the object width and were smaller and less variable, than for objects in the right visual field. Our results demonstrate that bimanual grasping is predominantly controlled by the right hemisphere, even in the context of grasping larger objects. |
K. M. Sharika; Sebastiaan F. W. Neggers; Tjerk P. Gutteling; Stefan Van der Stigchel; Hendrik Chris Dijkerman; A. Murthy Proactive control of sequential saccades in the human supplementary eye field Journal Article In: Proceedings of the National Academy of Sciences, vol. 110, no. 14, pp. E1311–E1320, 2013. @article{Sharika2013, Our ability to regulate behavior based on past experience has thus far been examined using single movements. However, natural behavior typically involves a sequence of movements. Here, we examined the effect of previous trial type on the concurrent planning of sequential saccades using a unique paradigm. The task consisted of two trial types: no-shift trials, which implicitly encouraged the concurrent preparation of the second saccade in a subsequent trial; and target-shift trials, which implicitly discouraged the same in the next trial. Using the intersaccadic interval as an index of concurrent planning, we found evidence for context-based preparation of sequential saccades. We also used functional MRI-guided, single-pulse, transcranial magnetic stimulation on human subjects to test the role of the supplementary eye field (SEF) in the proactive control of sequential eye movements. Results showed that (i) stimulating the SEF in the previous trial disrupted the previous trial type-based preparation of the second saccade in the nonstimulated current trial, (ii) stimulating the SEF in the current trial rectified the disruptive effect caused by stimulation in the previous trial, and (iii) stimulating the SEF facilitated the preparation of second saccades based on previous trial type even when the previous trial was not stimulated. Taken together, we show how the human SEF is causally involved in proactive preparation of sequential saccades. |
2012 |
José P. Ossandón; Selim Onat; Dario Cazzoli; Thomas Nyffeler; René M. Müri; Peter König Unmasking the contribution of low-level features to the guidance of attention Journal Article In: Neuropsychologia, vol. 50, no. 14, pp. 3478–3487, 2012. @article{Ossandon2012, The role of low-level stimulus-driven control in the guidance of overt visual attention has been difficult to establish because low- and high-level visual content are spatially correlated within natural visual stimuli. Here we show that impairment of parietal cortical areas, either permanently by a lesion or reversibly by repetitive transcranial magnetic stimulation (rTMS), leads to fixation of locations with higher values of low-level features as compared to control subjects or in a no-rTMS condition. Moreover, this unmasking of stimulus-driven control crucially depends on the intrahemispheric balance between top-down and bottom-up cortical areas. This result suggests that although in normal behavior high-level features might exert a strong influence, low-level features do contribute to guide visual selection during the exploration of complex natural stimuli. |
Marco Davare; A. Zénon; Gilles Pourtois; Michel Desmurget; Etienne Olivier Role of the medial part of the intraparietal sulcus in implementing movement direction Journal Article In: Cerebral Cortex, vol. 22, no. 6, pp. 1382–1394, 2012. @article{Davare2012, The contribution of the posterior parietal cortex (PPC) to visually guided movements has been originally inferred from observations made in patients suffering from optic ataxia. Subsequent electrophysiological studies in monkeys and functional imaging data in humans have corroborated the key role played by the PPC in sensorimotor transformations underlying goal-directed movements, although the exact contribution of this structure remains debated. Here, we used transcranial magnetic stimulation (TMS) to interfere transiently with the function of the left or right medial part of the intraparietal sulcus (mIPS) in healthy volunteers performing visually guided movements with the right hand. We found that a "virtual lesion" of either mIPS increased the scattering in initial movement direction (DIR), leading to longer trajectory and prolonged movement time, but only when TMS was delivered 100-160 ms before movement onset and for movements directed toward contralateral targets. Control experiments showed that deficits in DIR consequent to mIPS virtual lesions resulted from an inappropriate implementation of the motor command underlying the forthcoming movement and not from an inaccurate computation of the target localization. The present study indicates that mIPS plays a causal role in implementing specifically the direction vector of visually guided movements toward objects situated in the contralateral hemifield. |
Marc R. Kamke; Michelle G. Hall; Harley F. Lye; Martin V. Sale; Laura R. Fenlon; Timothy J. Carroll; Stephan Riek; Jason B. Mattingley Visual attentional load influences plasticity in the human motor cortex Journal Article In: Journal of Neuroscience, vol. 32, no. 20, pp. 7001–7008, 2012. @article{Kamke2012, Neural plasticity plays a critical role in learning, memory, and recovery from injury to the nervous system. Although much is known about the physical and physiological determinants of plasticity, little is known about the influence of cognitive factors. In this study, we investigated whether selective attention plays a role in modifying changes in neural excitability reflecting long-term potentiation (LTP)-like plasticity. We induced LTP-like effects in the hand area of the human motor cortex using transcranial magnetic stimulation (TMS). During the induction of plasticity, participants engaged in a visual detection task with either low or high attentional demands. Changes in neural excitability were assessed by measuring motor-evoked potentials in a small hand muscle before and after the TMS procedures. In separate experiments plasticity was induced either by paired associative stimulation (PAS) or intermittent theta-burst stimulation (iTBS). Because these procedures induce different forms of LTP-like effects, they allowed us to investigate the generality of any attentional influence on plasticity. In both experiments reliable changes in motor cortex excitability were evident under low-load conditions, but this effect was eliminated under high-attentional load. In a third experiment we investigated whether the attentional task was associated with ongoing changes in the excitability of motor cortex, but found no difference in evoked potentials across the levels of attentional load. Our findings indicate that in addition to their role in modifying sensory processing, mechanisms of attention can also be a potent modulator of cortical plasticity. |
Marc R. Kamke; Harrison E. Vieth; David Cottrell; Jason B. Mattingley Parietal disruption alters audiovisual binding in the sound-induced flash illusion Journal Article In: NeuroImage, vol. 62, no. 3, pp. 1334–1341, 2012. @article{Kamke2012a, Selective attention and multisensory integration are fundamental to perception, but little is known about whether, or under what circumstances, these processes interact to shape conscious awareness. Here, we used transcranial magnetic stimulation (TMS) to investigate the causal role of attention-related brain networks in multisensory integration between visual and auditory stimuli in the sound-induced flash illusion. The flash illusion is a widely studied multisensory phenomenon in which a single flash of light is falsely perceived as multiple flashes in the presence of irrelevant sounds. We investigated the hypothesis that extrastriate regions involved in selective attention, specifically within the right parietal cortex, exert an influence on the multisensory integrative processes that cause the flash illusion. We found that disruption of the right angular gyrus, but not of the adjacent supramarginal gyrus or of a sensory control site, enhanced participants' veridical perception of the multisensory events, thereby reducing their susceptibility to the illusion. Our findings suggest that the same parietal networks that normally act to enhance perception of attended events also play a role in the binding of auditory and visual stimuli in the sound-induced flash illusion. |
Ryota Kanai; Neil G. Muggleton; Vincent Walsh Transcranial direct current stimulation of the frontal eye fields during pro- and antisaccade tasks Journal Article In: Frontiers in Psychiatry, vol. 3, pp. 45, 2012. @article{Kanai2012, Transcranial direct current stimulation (tDCS) has been successfully applied to cortical areas such as the motor cortex and visual cortex. In the present study, we examined whether tDCS can reach and selectively modulate the excitability of the frontal eye field (FEF). In order to assess potential effects of tDCS, we measured saccade latency, landing point, and its variability in a simple prosaccade task and in an antisaccade task. In the prosaccade task, we found that anodal tDCS shortened the latency of saccades to a contralateral visual cue. However, cathodal tDCS did not show a significant modulation of saccade latency. In the antisaccade task, on the other hand, we found that the latency for ipisilateral antisaccades was prolonged during the stimulation, whereas anodal stimulation did not modulate the latency of antisaccades. In addition, anodal tDCS reduced the erroneous saccades toward the contralateral visual cue. These results in the antisaccade task suggest that tDCS modulates the function of FEF to suppress reflexive saccades to the contralateral visual cue. Both in the prosaccade and antisaccade tasks, we did not find any effect of tDCS on saccade landing point or its variability. Our present study is the first to show effects of tDCS over FEF and opens the possibility of applying tDCS for studying the functions of FEF in oculomotor and attentional performance. |
Kohitij Kar; Bart Krekelberg Transcranial electrical stimulation over visual cortex evokes phosphenes with a retinal origin Journal Article In: Journal of Neurophysiology, vol. 108, no. 8, pp. 2173–2178, 2012. @article{Kar2012, Transcranial electrical stimulation (tES) is a promising therapeutic tool for a range of neurological diseases. Understanding how the small currents used in tES spread across the scalp and penetrate the brain will be important for the rational design of tES therapies. Alternating currents applied transcranially above visual cortex induce the perception of flashes of light (phosphenes). This makes the visual system a useful model to study tES. One hypothesis is that tES generates phosphenes by direct stimulation of the cortex underneath the transcranial electrode. Here, we provide evidence for the alternative hypothesis that phosphenes are generated in the retina by current spread from the occipital electrode. Building on the existing literature, we first confirm that phosphenes are induced at lower currents when electrodes are placed farther away from visual cortex and closer to the eye. Second, we explain the temporal frequency tuning of phosphenes based on the well-known response properties of primate retinal ganglion cells. Third, we show that there is no difference in the time it takes to evoke phosphenes in the retina or by stimulation above visual cortex. Together, these findings suggest that phosphenes induced by tES over visual cortex originate in the retina. From this, we infer that tES currents spread well beyond the area of stimulation and are unlikely to lead to focal neural activation. Novel stimulation protocols that optimize current distributions are needed to overcome these limitations of tES. |
Wei-Kuang Liang; Chi-Hung Juan Modulation of motor control in saccadic behaviors by TMS over the posterior parietal cortex Journal Article In: Journal of Neurophysiology, vol. 108, no. 3, pp. 741–752, 2012. @article{Liang2012, The right posterior parietal cortex (rPPC) has been found to be critical in shaping visual selection and distractor-induced saccade curvature in the context of predictive as well as nonpredictive visual cues by means of transcranial magnetic stimulation (TMS) interference. However, the dynamic details of how distractor-induced saccade curvatures are affected by rPPC TMS have not yet been investigated. This study aimed to elucidate the key dynamic properties that cause saccades to curve away from distractors with different degrees of curvature in various TMS and target predictability conditions. Stochastic optimal feedback control theory was used to model the dynamics of the TMS saccade data. This allowed estimation of torques, which was used to identify the critical dynamic mechanisms producing saccade curvature. The critical mechanisms of distractor-induced saccade curvatures were found to be the motor commands and torques in the transverse direction. When an unpredictable saccade target occurred with rPPC TMS, there was an initial period of greater distractor-induced torque toward the side opposite the distractor in the transverse direction, immediately followed by a relatively long period of recovery torque that brought the deviated trace back toward the target. The results imply that the mechanisms of distractor-induced saccade curvature may be comprised of two mechanisms: the first causing the initial deviation and the second bringing the deviated trace back toward the target. The pattern of the initial torque in the transverse direction revealed the former mechanism. Conversely, the later mechanism could be well explained as a consequence of the control policy in this model. To summarize, rPPC TMS increased the initial torque away from the distractor as well as the recovery torque toward the target. |
2011 |
Neil G. Muggleton; Roger Kalla; Chi-Hung Juan; Vincent Walsh Dissociating the contributions of human frontal eye fields and posterior parietal cortex to visual search Journal Article In: Journal of Neurophysiology, vol. 105, no. 6, pp. 2891–2896, 2011. @article{Muggleton2011, Imaging, lesion, and transcranial magnetic stimulation (TMS) studies have implicated a number of regions of the brain in searching for a target defined by a combination of attributes. The necessity of both frontal eye fields (FEF) and posterior parietal cortex (PPC) in task performance has been shown by the application of TMS over these regions. The effects of stimulation over these two areas have, thus far, proved to be remarkably similar and the only dissociation reported being in the timing of their involvement. We tested the hypotheses that 1) FEF contributes to performance in terms of visual target detection (possibly by modulation of activity in extrastriate areas with respect to the target), and 2) PPC is involved in translation of visual information for action. We used a task where the presence (and location) of the target was indicated by an eye movement. Task disruption was seen with FEF TMS (with reduced accuracy on the task) but not with PPC stimulation. When a search task requiring a manual response was presented, disruption with PPC TMS was seen. These results show dissociation of FEF and PPC contributions to visual search performance and that PPC involvement seems to be dependent on the response required by the task, whereas this is not the case for FEF. This supports the idea of FEF involvement in visual processes in a manner that might not depend on the required response, whereas PPC seems to be involved when a manual motor response to a stimulus is required. |
Chang-Mao Chao; Philip Tseng; Tzu-Yu Hsu; Jia-Han Su; Ovid J. L. Tzeng; Daisy L. Hung; Neil G. Muggleton; Chi-Hung Juan Predictability of saccadic behaviors is modified by transcranial magnetic stimulation over human posterior parietal cortex Journal Article In: Human Brain Mapping, vol. 32, no. 11, pp. 1961–1972, 2011. @article{Chao2011, Predictability in the visual environment provides a powerful cue for efficient processing of scenes and objects. Recently, studies have suggested that the directionality and magnitude of saccade curvature can be informative as to how the visual system processes predictive information. The pres-ent study investigated the role of the right posterior parietal cortex (rPPC) in shaping saccade curva-tures in the context of predictive and non-predictive visual cues. We used an orienting paradigm that incorporated manipulation of target location predictability and delivered transcranial magnetic stimulation (TMS) over rPPC. Participants were presented with either an informative or uninforma-tive cue to upcoming target locations. Our results showed that rPPC TMS generally increased sac-cade latency and saccade error rates. Intriguingly, rPPC TMS increased curvatures away from the distractor only when the target location was unpredictable and decreased saccadic errors towards the distractor. These effects on curvature and accuracy were not present when the target location was predictable. These results dissociate the strong contingency between saccade latency and saccade curvature and also indicate that rPPC plays an important role in allocating and suppressing attention to distractors when the target demands visual disambiguation. Furthermore, the present study sug-gests that, like the frontal eye fields, rPPC is critically involved in determining saccade curvature and the generation of saccadic behaviors under conditions of differing target predictability. |
Zoï Kapoula; Qing Yang; Norman Sabbah; Marine Vernet Different effects of double-pulse TMS of the posterior parietal cortex on reflexive and voluntary saccades Journal Article In: Frontiers in Human Neuroscience, vol. 5, pp. 114, 2011. @article{Kapoula2011, Gap and overlap tasks are widely used to promote automatic versus controlled saccades. This study examines the hypothesis that the right posterior parietal cortex (PPC) is differently involved in the two tasks. Twelve healthy students participated in the experiment. We used double-pulse transcranial magnetic stimulation (dTMS) on the right PPC, the first pulse delivered at the target onset and the second 65 or 80 ms later. Each subject performed several blocks of gap or overlap task with or without dTMS. Eye movements were recorded with an Eyelink device. The results show an increase of latency of saccades after dTMS of the right PPC for both tasks but for different time windows (0-80 ms for the gap task, 0-65 ms for the overlap task). Moreover, for rightward saccades the coefficient of variation of latency increased in the gap task but decreased in the overlap task. Finally, in the gap task and for leftward saccades only, dTMS at 0-80 ms decreased the amplitude and the speed of saccades. Although the study is preliminary and needs further investigation in detail, the results support the hypothesis that the right PPC is involved differently in the initiation of the saccades for the two tasks: in the gap task the PPC controls saccade triggering while in the overlap task it could be a relay to the Frontal Eye Fields which is known to control voluntary saccades, e.g., memory-guided and perhaps the controlled saccades in the overlap task The results have theoretical and clinical significance as gap-overlap tasks are easy to perform even in advanced age and in patients with neurodegenerative diseases. |
Marine Vernet; Qing Yang; Zoï Kapoula Guiding binocular saccades during reading: A TMS study of the PPC Journal Article In: Frontiers in Human Neuroscience, vol. 5, pp. 14, 2011. @article{Vernet2011, Reading is an activity based on complex sequences of binocular saccades and fixations. During saccades, the eyes do not move together perfectly: saccades could end with a misalignment, compromising fused vision. During fixations, small disconjugate drift can partly reduce this misalignment. We hypothesized that maintaining eye alignment during reading involves active monitoring from posterior parietal cortex (PPC); this goes against traditional views considering only downstream binocular control. Nine young adults read a text; transcranial magnetic stimulation (TMS) was applied over the PPC every 5 ± 0.2 s. Eye movements were recorded binocularly with Eyelink II. Stimulation had three major effects: (1) disturbance of eye alignment during fixation; (2) increase of saccade disconjugacy leading to eye misalignment; (3) decrease of eye alignment reduction during fixation drift. The effects depend on the side; the right PPC was more involved in maintaining alignment over the motor sequence. Thus, the PPC is actively involved in the control of binocular eye alignment during reading, allowing clear vision. Cortical activation during reading is related to linguistic processes and motor control per se. The study might be of interest for the understanding of deficits of binocular coordination, encountered in several populations, e.g., in children with dyslexia. |
Minnan Xu-Wilson; Jing Tian; Reza Shadmehr; David S. Zee TMS perturbs saccade trajectories and unmasks an internal feedback controller for saccades Journal Article In: Journal of Neuroscience, vol. 31, no. 32, pp. 11537–11546, 2011. @article{XuWilson2011, When we applied a single pulse of transcranial magnetic stimulation (TMS) to any part of the human head during a saccadic eye movement, the ongoing eye velocity was reduced as early as 45 ms after the TMS, and lasted ∼32 ms. The perturbation to the saccade trajectory was not due to a mechanical effect of the lid on the eye (e.g., from blinks). When the saccade involved coordinated movements of both the eyes and the lids, e.g., in vertical saccades, TMS produced a synchronized inhibition of the motor commands to both eye and lid muscles. The TMS-induced perturbation of the eye trajectory did not show habituation with repetition, and was present in both pro-saccades and anti-saccades. Despite the perturbation, the eye trajectory was corrected within the same saccade with compensatory motor commands that guided the eyes to the target. This within-saccade correction did not rely on visual input, suggesting that the brain monitored the oculomotor commands as the saccade unfolded, maintained a real-time estimate of the position of the eyes, and corrected for the perturbation. TMS disrupted saccades regardless of the location of the coil on the head, suggesting that the coil discharge engages a nonhabituating startle-like reflex system. This system affects ongoing motor commands upstream of the oculomotor neurons, possibly at the level of the superior colliculus or omnipause neurons. Therefore, a TMS pulse centrally perturbs saccadic motor commands, which are monitored possibly via efference copy and are corrected via internal feedback. |
Qing Yang; Zoï Kapoula Distinct control of initiation and metrics of memory-guided saccades and vergence by the FEF: A TMS study Journal Article In: PLoS ONE, vol. 6, no. 5, pp. e20322, 2011. @article{Yang2011, BACKGROUND: The initiation of memory guided saccades is known to be controlled by the frontal eye field (FEF). Recent physiological studies showed the existence of an area close to FEF that controls also vergence initiation and execution. This study is to explore the effect of transcranial magnetic simulation (TMS) over FEF on the control of memory-guided saccade-vergence eye movements. METHODOLOGY/PRINCIPAL FINDINGS: Subjects had to make an eye movement in dark towards a target flashed 1 sec earlier (memory delay); the location of the target relative to fixation point was such as to require either a vergence along the median plane, or a saccade, or a saccade with vergence; trials were interleaved. Single pulse TMS was applied on the left or right FEF; it was delivered at 100 ms after the end of memory delay, i.e. extinction of fixation LED that was the "go" signal. Twelve healthy subjects participated in the study. TMS of left or right FEF prolonged the latency of all types of eye movements; the increase varied from 21 to 56 ms and was particularly strong for the divergence movements. This indicates that FEF is involved in the initiation of all types of memory guided movement in the 3D space. TMS of the FEF also altered the accuracy but only for leftward saccades combined with either convergence or divergence; intrasaccadic vergence also increased after TMS of the FEF. CONCLUSIONS/SIGNIFICANCE: The results suggest anisotropy in the quality of space memory and are discussed in the context of other known perceptual motor anisotropies. |
2010 |
Ben M. Harvey; O. J. Braddick; A. Cowey In: Journal of Vision, vol. 10, no. 5, pp. 1–15, 2010. @article{Harvey2010, Our recent psychophysical experiments have identified differences in the spatial summation characteristics of pattern detection and position discrimination tasks performed with rotating, expanding, and contracting stimuli. Areas MT and MST are well established to be involved in processing these stimuli. fMRI results have shown retinotopic activation of area V3A depending on the location of the center of radial motion in vision. This suggests the possibility that V3A may be involved in position discrimination tasks with these motion patterns. Here we use repetitive transcranial magnetic stimulation (rTMS) over MT+ and a dorsomedial extrastriate region including V3A to try to distinguish between TMS effects on pattern detection and position discrimination tasks. If V3A were involved in position discrimination, we would expect to see effects on position discrimination tasks, but not pattern detection tasks, with rTMS over this dorsomedial extrastriate region. In fact, we could not dissociate TMS effects on the two tasks, suggesting that they are performed by the same extrastriate area, in MT+. |
Steven L. Prime; Michael Vesia; J. Douglas Crawford TMS over human frontal eye fields disrupts trans-saccadic memory of multiple objects Journal Article In: Cerebral Cortex, vol. 20, no. 4, pp. 759–772, 2010. @article{Prime2010, We recently showed that transcranial magnetic stimulation (TMS) over the right parietal eye fields disrupts memory of object features and locations across saccades. We applied TMS over the frontal eye fields (FEF) as subjects compared the feature details of visual targets presented either within a single eye fixation (Fixation Task) or across a saccade (Saccade Task). TMS pulses were randomly delivered at one of 3 time intervals around the time of the saccade, or at equivalent times in the Fixation Task. A No-TMS control confirmed that subjects could normally retain approximately 3 visual features. TMS in the Fixation Task had no effect compared with No-TMS, but differences among TMS times were found during right FEF stimulation. TMS over either the right or left FEF disrupted memory performance in the Saccade Task when stimulation coincided most closely with the saccade. The capacity to compare pre-and postsaccadic features was reduced to 1-2 objects, as expected if the spatial aspect of memory was disrupted. These findings suggest that the FEF plays a role in the spatial processing involved in trans-saccadic memory of visual features. We propose that this process employs saccade-related feedback signals similar to those observed in spatial updating. |
Michael Vesia; Steven L. Prime; Xiaogang Yan; Lauren E. Sergio; J. Douglas Crawford Specificity of human parietal saccade and reach regions during transcranial magnetic stimulation Journal Article In: Journal of Neuroscience, vol. 30, no. 39, pp. 13053–13065, 2010. @article{Vesia2010, Single-unit recordings in macaque monkeys have identified effector-specific regions in posterior parietal cortex (PPC), but functional neuroimaging in the human has yielded controversial results. Here we used on-line repetitive transcranial magnetic stimulation (rTMS) to determine saccade and reach specificity in human PPC. A short train of three TMS pulses (separated by an interval of 100 ms) was delivered to superior parieto-occipital cortex (SPOC), a region over the midposterior intraparietal sulcus (mIPS), and a site close to caudal IPS situated over the angular gyrus (AG) during a brief memory interval while subjects planned either a saccade or reach with the left or right hand. Behavioral measures then were compared to controls without rTMS. Stimulation of mIPS and AG produced similar patterns: increased end-point variability for reaches and decreased saccade accuracy for contralateral targets. In contrast, stimulation of SPOC deviated reach end points toward visual fixation and had no effect on saccades. Contralateral-limb specificity was highest for AG and lowest for SPOC. Visual feedback of the hand negated rTMS-induced disruptions of the reach plan for mIPS and AG, but not SPOC. These results suggest that human SPOC is specialized for encoding retinally peripheral reach goals, whereas more anterior-lateral regions (mIPS and AG) along the IPS possess overlapping maps for saccade and reach planning and are more closely involved in motor details (i.e., planning the reach vector for a specific hand). This work provides the first causal evidence for functional specificity of these parietal regions in healthy humans. |
Michael L. Waterston; Christopher C. Pack Improved discrimination of visual stimuli following repetitive transcranial magnetic stimulation Journal Article In: PLoS ONE, vol. 5, no. 4, pp. e10354, 2010. @article{Waterston2010, Repetitive transcranial magnetic stimulation (rTMS) at certain frequencies increases thresholds for motor-evoked potentials and phosphenes following stimulation of cortex. Consequently rTMS is often assumed to introduce a “virtual lesion” in stimulated brain regions, with correspondingly diminished behavioral performance. Here we investigated the effects of rTMS to visual cortex on subjects' ability to perform visual psychophysical tasks. Contrary to expectations of a visual deficit, we find that rTMS often improves the discrimination of visual features. For coarse orientation tasks, discrimination of a static stimulus improved consistently following theta-burst stimulation of the occipital lobe. Using a reaction-time task, we found that these improvements occurred throughout the visual field and lasted beyond one hour post-rTMS. Low-frequency (1 Hz) stimulation yielded similar improvements. In contrast, we did not find consistent effects of rTMS on performance in a fine orientation discrimination task. Overall our results suggest that rTMS generally improves or has no effect on visual acuity, with the nature of the effect depending on the type of stimulation and the task. We interpret our results in the context of an ideal-observer model of visual perception. |
2009 |
Ulrich Nuding; Roger Kalla; Neil G. Muggleton; Ulrich Büttner; Vincent Walsh; Stefan Glasauer TMS evidence for smooth pursuit gain control by the frontal eye fields Journal Article In: Cerebral Cortex, vol. 19, no. 5, pp. 1144–1150, 2009. @article{Nuding2009, Smooth pursuit eye movements are used to continuously track slowly moving visual objects. A peculiar property of the smooth pursuit system is the nonlinear increase in sensitivity to changes in target motion with increasing pursuit velocities. We investigated the role of the frontal eye fields (FEFs) in this dynamic gain control mechanism by application of transcranial magnetic stimulation. Subjects were required to pursue a slowly moving visual target whose motion consisted of 2 components: a constant velocity component at 4 different velocities (0, 8, 16, and 24 deg/s) and a superimposed high-frequency sinusoidal oscillation (4 Hz, +/-8 deg/s). Magnetic stimulation of the FEFs reduced not only the overall gain of the system, but also the efficacy of the dynamic gain control. We thus provide the first direct evidence that the FEF population is significantly involved in the nonlinear computation necessary for continuously adjusting the feedforward gain of the pursuit system. We discuss this with relation to current models of smooth pursuit. |
Roger Kalla; Neil G. Muggleton; Alan Cowey; Vincent Walsh Human dorsolateral prefrontal cortex is involved in visual search for conjunctions but not features: A theta TMS study Journal Article In: Cortex, vol. 45, no. 9, pp. 1085–1090, 2009. @article{Kalla2009, Functional neuroimaging studies have shown that the detection of a target defined by more than one feature (for example, a conjunction of colour and orientation) amongst distractors is associated with the activation of a network of brain areas. Dorsolateral prefrontal cortex (DLPFC), along with areas such as the frontal eye fields (FEF) and posterior parietal cortex (PPC), is a component of this network. While transcranial magnetic stimulation (TMS) had shown that both FEF and PPC are necessary for, and not just correlated with, successful conjunction search, this is not the case for DLPFC. To test the hypothesis that this area is also necessary for efficient conjunction search, TMS was applied over DLPFC and the effects on conjunction and feature (in this case colour) search performance compared with those when TMS was delivered over area MT/V5 and a vertex control stimulation condition. DLPFC TMS impaired performance on the conjunction search task but was without effect on feature search, similar to findings when TMS is delivered over PPC or FEF. Vertex TMS had no effects whereas MT/V5 TMS significantly improved performance with a time course that may indicate that this was due to modulation of V4 activity. These findings illustrate that, like FEF and PPC, DLPFC is necessary for fully effective conjunction visual search performance. |
Clive R. Rosenthal; Emma E. Roche-Kelly; Masud Husain; Christopher Kennard Response-dependent contributions of human primary motor cortex and angular gyrus to manual and perceptual sequence learning Journal Article In: Journal of Neuroscience, vol. 29, no. 48, pp. 15115–15125, 2009. @article{Rosenthal2009, Motor sequence learning on the serial reaction time task involves the integration of response-, stimulus-, and effector-based information. Human primary motor cortex (M1) and the inferior parietal lobule (IPL) have been identified with supporting the learning of effector-dependent and -independent information, respectively. Current neurocognitive data are, however, exclusively based on learning complex sequence information via perceptual-motor responses. Here, we investigated the effects of continuous theta-burst transcranial magnetic stimulation (cTBS)-induced disruption of M1 and the angular gyrus (AG) of the IPL on learning a probabilistic sequence via sequential perceptual-motor responses (experiment 1) or covert orienting of visuospatial attention (experiment 2). Functional effects on manual sequence learning were evident during 75% of training trials in the cTBS M1 condition, whereas cTBS over the AG resulted in interference confined to a midpoint during the training phase. Posttraining direct (declarative) tests of sequence knowledge revealed that cTBS over M1 modulated the availability of newly acquired sequence knowledge, whereby sequence knowledge was implicit in the cTBS M1 condition but was available to conscious awareness in the cTBS AG and control conditions. In contrast, perceptual sequence learning was abolished in the perceptual cTBS AG condition, whereas learning was intact and available to conscious awareness in the cTBS M1 and control conditions. These results show that the right AG had a critical role in perceptual sequence learning, whereas M1 had a causal role in developing experience-dependent functional attributes relevant to conscious knowledge on manual but not perceptual sequence learning. |
Helene M. Ettinger-Veenstra; W. Huijbers; Tjerk P. Gutteling; M. Vink; J. Leon Kenemans; Sebastiaan F. W. Neggers In: Journal of Neurophysiology, vol. 102, no. 6, pp. 3469–3480, 2009. @article{EttingerVeenstra2009, It is well known that parts of a visual scene are prioritized for visual processing, depending on the current situation. How the CNS moves this focus of attention across the visual image is largely unknown, although there is substantial evidence that preparation of an action is a key factor. Our results support the view that direct corticocortical feedback connections from frontal oculomotor areas to the visual cortex are responsible for the coupling between eye movements and shifts of visuospatial attention. Functional magnetic resonance imaging (fMRI)-guided transcranial magnetic stimulation (TMS) was applied to the frontal eye fields (FEFs) and intraparietal sulcus (IPS). A single pulse was delivered 60, 30, or 0 ms before a discrimination target was presented at, or next to, the target of a saccade in preparation. Results showed that the known enhancement of discrimination performance specific to locations to which eye movements are being prepared was enhanced by early TMS on the FEF contralateral to eye movement direction, whereas TMS on the IPS resulted in a general performance increase. The current findings indicate that the FEF affects selective visual processing within the visual cortex itself through direct feedback projections. |
Robin Walker; Puncharat Techawachirakul; Patrick Haggard Frontal eye field stimulation modulates the balance of salience between target and distractors Journal Article In: Brain Research, vol. 1270, pp. 54–63, 2009. @article{Walker2009, Natural scenes generally include several possible objects that can be the target for a shift of gaze and attention. The oculomotor system may select a single target by boosting neural activation representing the target, and also by inhibiting neural activity associated with competing alternatives (distractors). We examine the role of the frontal eye field (FEF) in these processes through the effects of single-pulse transcranial magnetic stimulation (TMS) on the distractor-related modulation of saccade trajectories. Participants made voluntary saccades to peripheral locations specified by a central arrow-cue. On some trials, visual distractors appeared remote from the target location. The competing distractor produced a deviation of saccade trajectory, away from the distractor location. Single-pulse TMS stimulation of the right frontal eye field increased this distractor-related deviation compared that observed when stimulation was applied to a control site (vertex). The increase in distractor-related deviation of trajectory, following FEF stimulation, was observed for saccades made in both the left and right visual fields and could not be attributed to an effect of TMS on saccade latency. The enhanced distractor-related deviation following FEF stimulation could reflect increased inhibition of the competing distractor, or reduced salience of the endogenous saccade goal. The results are interpreted in light of neurophysiological evidence that the human FEF is involved in the dynamic interaction between competing stimuli for the selection of a candidate target. |
2008 |
Thomas Nyffeler; Dario Cazzoli; Pascal Wurtz; Mathias Lüthi; Roman Von Wartburg; Silvia Chaves; Anouk Déruaz; Christian W. Hess; René M. Müri Neglect-like visual exploration behaviour after theta burst transcranial magnetic stimulation of the right posterior parietal cortex Journal Article In: European Journal of Neuroscience, vol. 27, no. 7, pp. 1809–1813, 2008. @article{Nyffeler2008, The right posterior parietal cortex (PPC) is critically involved in visual exploration behaviour, and damage to this area may lead to neglect of the left hemispace. We investigated whether neglect-like visual exploration behaviour could be induced in healthy subjects using theta burst repetitive transcranial magnetic stimulation (rTMS). To this end, one continuous train of theta burst rTMS was applied over the right PPC in 12 healthy subjects prior to a visual exploration task where colour photographs of real-life scenes were presented on a computer screen. In a control experiment, stimulation was also applied over the vertex. Eye movements were measured, and the distribution of visual fixations in the left and right halves of the screen was analysed. In comparison to the performance of 28 control subjects without stimulation, theta burst rTMS over the right PPC, but not the vertex, significantly decreased cumulative fixation duration in the left screen-half and significantly increased cumulative fixation duration in the right screen-half for a time period of 30 min. These results suggest that theta burst rTMS is a reliable method of inducing transient neglect-like visual exploration behaviour. |
Roger Kalla; Neil G. Muggleton; Chi-Hung Juan; Alan Cowey; Vincent Walsh The timing of the involvement of the frontal eye fields and posterior parietal cortex in visual search Journal Article In: NeuroReport, vol. 19, no. 10, pp. 1069–1073, 2008. @article{Kalla2008, The frontal eye fields (FEFs) and posterior parietal cortex (PPC) are important for target detection in conjunction visual search but the relative timings of their contribution have not been compared directly. We addressed this using temporally specific double pulse transcranial magnetic stimulation delivered at different times over FEFs and PPC during performance of a visual search task. Disruption of performance was earlier (0/40 ms) with FEF stimulation than with PPC stimulation (120/160 ms), revealing a clear and substantial temporal dissociation of the involvement of these two areas in conjunction visual search. We discuss these timings with reference to the respective roles of FEF and PPC in the modulation of extrastriate visual areas and selection of responses. |
Marine Vernet; Qing Yang; Gintautas Daunys; Christophe Orssaud; Thomas Eggert; Zoï Kapoula How the brain obeys Hering's law: A TMS study of the posterior parietal cortex Journal Article In: Investigative Ophthalmology & Visual Science, vol. 49, no. 1, pp. 230–237, 2008. @article{Vernet2008, PURPOSE: Human ocular saccades are not perfectly yoked; the origin of this disconjugacy (muscular versus central) remains controversial. The purpose of this study was to test a cortical influence on the binocular coordination of saccades. METHODS: The authors used a gap paradigm to elicit vertical or horizontal saccades of 10 degrees , randomly interleaved; transcranial magnetic stimulation (TMS) was applied on the posterior parietal cortex (PPC) 100 ms after the target onset. RESULTS: TMS of the left or right PPC increased (i) the misalignment of the eyes during the presaccadic fixation period; (ii) the size difference between the saccades of the eyes, called disconjugacy; the increase of disconjugacy was significant for rightward and downward saccades after TMS of the right PPC and for downward saccades after TMS of the left PPC. CONCLUSIONS: The authors conclude that the PPC is actively involved in maintaining eye alignment during fixation and in the control of binocular coordination of saccades. |
Marine Vernet; Qing Yang; Gintautas Daunys; Christophe Orssaud; Zoï Kapoula TMS of the posterior parietal cortex delays the latency of unpredictable saccades but not when they are combined with predictable divergence Journal Article In: Brain Research Bulletin, vol. 76, no. 1-2, pp. 50–56, 2008. @article{Vernet2008a, This study tests the influence of transcranial magnetic stimulation (TMS) of the posterior parietal cortex (PPC) on the initiation of horizontal and vertical saccades, alone or combined with a predictable divergence. A gap paradigm was used; TMS was applied 100 ms after target onset. TMS of the left PPC increased the latency of unpredictable rightward saccades, while TMS of the right PPC increased the latency of unpredictable downward saccades. Yet, when unpredictable saccades were combined with predictable divergence, neither component was affected. We suggest that in the latter case, the initiation of both components was taken in charge by another area, e.g. frontal. Thus, even when one component was predictable, a common mechanism controls the initiation of both components. The results confirm that TMS only modifies the latency when the cortical area stimulated is involved in the triggering of the eye movement. |
2007 |
Sebastiaan F. W. Neggers; W. Huijbers; C. M. Vrijlandt; Björn N. S. Vlaskamp; D. J. L. G. Schutter; J. Leon Kenemans TMS pulses on the frontal eye fields break coupling between visuospatial attention and eye movements Journal Article In: Journal of Neurophysiology, vol. 98, no. 5, pp. 2765–2778, 2007. @article{Neggers2007, While preparing a saccadic eye movement, visual processing of the saccade goal is prioritized. Here, we provide evidence that the frontal eye fields (FEFs) are responsible for this coupling between eye movements and shifts of visuospatial attention. Functional magnetic resonance imaging (fMRI)-guided transcranial magnetic stimulation (TMS) was applied to the FEFs 30 ms before a discrimination target was presented at or next to the target of a saccade in preparation. Results showed that the well-known enhancement of discrimination performance on locations to which eye movements are being prepared was diminished by TMS contralateral to eye movement direction. Based on the present and other reports, we propose that saccade preparatory processes in the FEF affect selective visual processing within the visual cortex through feedback projections, in that way coupling saccade preparation and visuospatial attention. |
Samuel B. Hutton; Brendan S. Weekes Low frequency rTMS over posterior parietal cortex impairs smooth pursuit eye tracking Journal Article In: Experimental Brain Research, vol. 183, no. 2, pp. 195–200, 2007. @article{Hutton2007, The role of the posterior parietal cortex in smooth pursuit eye movements remains unclear. We used low frequency repetitive transcranial magnetic stimulation (rTMS) to study the cognitive and neural systems involved in the control of smooth pursuit eye movements. Eighteen participants were tested on two separate occasions. On each occasion we measured smooth pursuit eye tracking before and after 6 min of 1 Hz rTMS delivered at 90% of motor threshold. Low frequency rTMS over the posterior parietal cortex led to a significant reduction in smooth pursuit velocity gain, whereas rTMS over the motor cortex had no effect on gain. We conclude that low frequency offline rTMS is a potentially useful tool with which to explore the cortical systems involved in oculomotor control. |