Felix Duecker

Hemispheric differences in the voluntary control of spatial attention: Direct evidence for a right-hemispheric dominance within frontal cortex

Lesion studies in neglect patients have inspired two competing models of spatial attention control, namely, Heilmans “hemispatial” theory and Kinsbournes “opponent processor” model. Both assume a functional asymmetry between the two hemispheres but propose very different mechanisms. Neuroimaging studies have identified a bilateral dorsal frontoparietal network underlying voluntary shifts of spatial attention. However, lateralization of attentional processes within this network has not been consistently reported. In the current study, we aimed to provide direct evidence concerning the functional asymmetry of the right and left FEF during voluntary shifts of spatial attention. To this end, we applied fMRI-guided neuronavigation to disrupt individual FEF activation foci with a longer-lasting inhibitory patterned TMS protocol followed by a spatial cueing task. Our results indicate that right FEF stimulation impaired the ability of shifting spatial attention toward both hemifields, whereas the effects of left FEF stimulation were limited to the contralateral hemifield. These results provide strong direct evidence for right-hemispheric dominance in spatial attention within frontal cortex supporting Heilmans “hemispatial” theory. This complements previous TMS studies that generally conform to Kinsbournes “opponent processor” model after disruption of parietal cortex, and we therefore propose that both theories are not mutually exclusive.

Rethinking the role of sham TMS

Sham transcranial magnetic stimulation (TMS) approaches are widely used in basic and clinical research to ensure that observed effects are due to the intended neural manipulation instead of being caused by various possible side effects. We here critically discuss several methodological aspects of sham TMS. Importantly, we propose to carefully distinguish between the placebo versus sensory side effects of TMS. In line with this conceptual distinction, we describe current limitations of sham TMS approaches in the context of placebo effects and blinding success, followed by a short review of our own work demonstrating that the sensory side effects of sham TMS are not unspecific as often falsely assumed. Lastly, we argue that sham TMS approaches are inherently insufficient as full-fledged control conditions as they fail to demonstrate the specificity of TMS effects to a particular brain area or time point of stimulation. Sham TMS should therefore only complement alternative control strategies in TMS research.

The hybrid model of attentional control : new insights into hemispheric asymmetries inferred from TMS research

Several competing theories on the mechanisms underlying attentional control have emerged over the years that, despite their substantial differences, all emphasize the importance of hemispheric asymmetries. Transcranial magnetic stimulation (TMS) has proven particularly successful in teasing them apart by selective perturbation of the dorsal and ventral fronto-parietal network. We here critically review the TMS literature and show that hemispheric asymmetries within the dorsal attention network differ between parietal and frontal cortex. Specifically, posterior parietal cortex seems to be characterized by a contralateral bias of each hemisphere and competition between them. In contrast, the right frontal eye field seems to be involved in shifting attention toward both hemifields, whereas left frontal eye field is only involved on shifting attention toward the contralateral hemifield. In the light of presented evidence, we propose to revise the functional-anatomical model originally proposed by Corbetta and Shulman (2011, 2002) and introduce a hybrid model of hemispheric asymmetries in attentional control.

Pre-Stimulus Sham TMS Facilitates Target Detection

Transcranial magnetic stimulation (TMS) allows non-invasive manipulation of brain activity during active task performance. Because every TMS pulse is accompanied by non-neural effects such as a clicking sound and somato-sensation on the head, control conditions are required to ensure that changes in task behavior are indeed due to the induced neural effects. However, the non-neural effects of TMS in the context of a given task performance are largely unknown and, consequently, it is unclear what constitutes a valid control condition. We explored the non-neural effects of TMS on visual target detection. Participants received single pulse sham TMS to each hemisphere at different time points prior to target appearance during a visual target detection task. It was hypothesized that the clicking sound of a sham TMS pulse differentially affects performance depending on the location of the coil and the timing of the pulse.Our results show that, first, sham TMS caused a facilitation of reaction times when preceding the target stimulus by 150, 200, and 250 ms, whereas earlier and later time windows were not effective. Second, positioning the TMS coil ipsilateral instead of contralateral relative to the target stimulus improved reaction times. Third, infrequent noTMS trials that were interleaved with sham TMS trials had oddball-like properties resulting in increased reaction times during noTMS. The clicking sound produced by sham TMS influences task performance in multiple ways. These non-neural effects of TMS need to be controlled for in TMS research and the present findings provide an empirical basis for deciding what constitutes a valid control condition.

Time- and task-dependent non-neural effects of real and sham TMS.

Transcranial magnetic stimulation (TMS) is widely used in experimental brain research to manipulate brain activity in humans. Next to the intended neural effects, every TMS pulse produces a distinct clicking sound and sensation on the head which can also influence task performance. This necessitates careful consideration of control conditions in order to ensure that behavioral effects of interest can be attributed to the neural consequences of TMS and not to non-neural effects of a TMS pulse. Surprisingly, even though these non-neural effects of TMS are largely unknown, they are often assumed to be unspecific, i.e. not dependent on TMS parameters. This assumption is inherent to many control strategies in TMS research but has recently been challenged on empirical grounds. Here, we further develop the empirical basis of control strategies in TMS research. We investigated the time-dependence and task-dependence of the non-neural effects of TMS and compared real and sham TMS over vertex. Critically, we show that non-neural TMS effects depend on a complex interplay of these factors. Although TMS had no direct neural effects, both pre- and post-stimulus TMS time windows modulated task performance on both a sensory detection task and a cognitive angle judgment task. For the most part, these effects were quantitatively similar across tasks but effect sizes were clearly different. Moreover, the effects of real and sham TMS were almost identical with interesting exceptions that shed light on the relative contribution of auditory and somato-sensory aspects of a TMS pulse. Knowledge of such effects is of critical importance for the interpretation of TMS experiments and helps deciding what constitutes an appropriate control condition. Our results broaden the empirical basis of control strategies in TMS research and point at potential pitfalls that should be avoided.

Early stages of motor skill learning and the specific relevance of the cortical motor system - a combined behavioural training and theta burst TMS study

PURPOSE To examine whether motor performance and motor learning in healthy subjects can be segregated into a number of distinct motor abilities which are linked to intact processing in different motor-related brain regions (M1, S1, SMA, PMC) early during learning. METHODS Seven young healthy subjects trained in eight motor arm tasks (Arm Ability Training, AAT) once a day for 5 days using their left non-dominant arm. Except for day 1 (baseline), training was performed before and after applying an inhibitory form of repetitive transcranial magnetic stimulation (cTBS, continuous theta burst) to either M1, S1, SMA, or PMC. RESULTS A principal component analysis of the motor behaviour data suggested four independent motor abilities: aiming, speed, steadiness, and visuomotor tracking. AAT induced substantial motor learning across abilities. Within session effects of cTBS revealed that activity in primary somatosensory cortex (S1) was relevant for motor performance and learning across all tasks whereas M1 was specifically involved in rapid tapping movements, PMC in ballistic arm navigation in extra-personal space; performance on a non-trained motor tasks was not affected by cTBS. CONCLUSIONS Cortical sensory and motor areas including S1, M1, and PMC functionally contribute to early motor learning in a differential manner across motor abilities.

Horizontal tuning for faces originates in high-level Fusiform Face Area

Recent work indicates that the specialization of face visual perception relies on the privileged processing of horizontal angles of facial information. This suggests that stimulus properties assumed to be fully resolved in primary visual cortex (V1; e.g., orientation) in fact determine human vision until high-level stages of processing. To address this hypothesis, the present fMRI study explored the orientation sensitivity of V1 and high-level face-specialized ventral regions such as the Occipital Face Area (OFA) and Fusiform Face Area (FFA) to different angles of face information. Participants viewed face images filtered to retain information at horizontal, vertical or oblique angles. Filtered images were viewed upright, inverted and (phase-)scrambled. FFA responded most strongly to the horizontal range of upright face information; its activation pattern reliably separated horizontal from oblique ranges, but only when faces were upright. Moreover, activation patterns induced in the right FFA and the OFA by upright and inverted faces could only be separated based on horizontal information. This indicates that the specialized processing of upright face information in the OFA and FFA essentially relies on the encoding of horizontal facial cues. This pattern was not passively inherited from V1, which was found to respond less strongly to horizontal than other orientations likely due to adaptive whitening. Moreover, we found that orientation decoding accuracy in V1 was impaired for stimuli containing no meaningful shape. By showing that primary coding in V1 is influenced by high-order stimulus structure and that high-level processing is tuned to selective ranges of primary information, the present work suggests that primary and high-level levels of the visual system interact in order to modulate the processing of certain ranges of primary information depending on their relevance with respect to the stimulus and task at hand.

Thinking caps for everyone? The role of neuro-enhancement by non-invasive brain stimulation in neuroscience and beyond

Neuro-enhancement by non-invasive brain stimulation (NIBS) has recently made considerable progress, triggering discussions regarding future applications to enhance human performance. We show that neuroscientific research does not aim at improving brain functions per se. Instead, neuro-enhancement is a research tool that has great potential to reveal the neural mechanisms underlying perception, cognition, and behavior. We provide instructive examples that showcase the relevance of neuro-enhancement by NIBS in neuroscience. Importantly, we argue that the scientific value of neuro-enhancement critically depends on our understanding of why enhancing effects occur. This is in contrast to applications of neuro-enhancement in other domains, where such knowledge may not be required. We conclude that neuro-enhancement as a therapeutic tool or in healthy people outside of neuroscience should be kept conceptually distinct, as these are separate domains with entirely different motives for enhancing human performance. Consequently, the underlying principles that justify the application of NIBS will be different in each domain and arguments for or against neuro-enhancement in one domain do not necessarily generalize to other domains.

The cortex-based alignment approach to tms coil positioning

TMS allows noninvasive manipulation of brain activity in healthy participants and patients. The effectiveness of TMS experiments critically depends on precise TMS coil positioning, which is best for most brain areas when a frameless stereotactic system is used to target activation foci based on individual fMRI data. From a purely scientific perspective, individual fMRI-guided TMS is thus the method of choice to ensure optimal TMS efficiency. Yet, from a more practical perspective, such individual functional data are not always available, and therefore alternative TMS coil positioning approaches are often applied, for example, based on functional group data reported in Talairach coordinates. We here propose a novel method for TMS coil positioning that is based on functional group data, yet only requires individual anatomical data. We used cortex-based alignment (CBA) to transform individual anatomical data to an atlas brain that includes probabilistic group maps of two functional regions (FEF and hMT+/V5). Then, these functional group maps were back-transformed to the individual brain anatomy, preserving functional–anatomical correspondence. As a proof of principle, the resulting CBA-based functional targets in individual brain space were compared with individual FEF and hMT+/V5 hotspots as conventionally localized with individual fMRI data and with targets based on Talairach coordinates as commonly done in TMS research in case only individual anatomical data are available. The CBA-based approach significantly improved localization of functional brain areas compared with traditional Talairach-based targeting. Given the widespread availability of CBA schemes and preexisting functional group data, the proposed procedure is easy to implement and at no additional measurement costs. However, the accuracy of individual fMRI-guided TMS remains unparalleled, and the CBA-based approach should only be the method of choice when individual functional data cannot be obtained or experimental factors argue against it.

Spatially specific vs. unspecific disruption of visual orientation perception using chronometric pre-stimulus TMS

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.