Our results provide causal evidence that circuits originating in the human FEF can modulate activity in retinotopic visual cortex, in a manner that differentiates the central and peripheral visual field, with functional consequences for perception. More generally, our study illustrates how the new approach of concurrent TMS-fMRI can now reveal causal interactions between remote but interconnected areas of the human brain.
It has often been proposed that regions of the human parietal and/or frontal lobe may modulate activity in visual cortex, for example, during selective attention or saccade preparation. However, direct evidence for such causal claims is largely missing in human studies, and it remains unclear to what degree the putative roles of parietal and frontal regions in modulating visual cortex may differ. Here we used transcranial magnetic stimulation (TMS) and functional magnetic resonance imaging (fMRI) concurrently, to show that stimulating right human intraparietal sulcus (IPS, at a site previously implicated in attention) elicits a pattern of activity changes in visual cortex that strongly depends on current visual context. Increased intensity of IPS TMS affected the blood oxygen level-dependent (BOLD) signal in V5/MT+ only when moving stimuli were present to drive this visual region, whereas TMS-elicited BOLD signal changes were observed in areas V1-V4 only during the absence of visual input. These influences of IPS TMS upon remote visual cortex differed significantly from corresponding effects of frontal (eye field) TMS, in terms of how they related to current visual input and their spatial topography for retinotopic areas V1-V4. Our results show directly that parietal and frontal regions can indeed have distinct patterns of causal influence upon functional activity in human visual cortex.
Localized repetitive transcranial magnetic stimulation was used to disrupt visuospatial perception in the near and far space of six healthy volunteer subjects. In addition to the baseline condition, they were stimulated over the right posterior parietal cortex, the right or left dorsal occipital cortex or the right ventral occipital cortex, during the brief presentation of a transected horizontal line. Subjects had to indicate whether the part of the line to the left or right of the transection appeared longer. The stimulus display was back-projected on a screen at a viewing distance of either 50 or 150 cm ("near" and "far" space, respectively). Reaction times and choices were measured. In a forced-choice paradigm, subjects showed "pseudoneglect", the natural tendency of neurologically intact subjects to perceive the left side of a centrally transected line as slightly longer than the right. These errors occurred more for lines in near space than for lines in far space. Magnetic stimulation of the right posterior parietal cortex or the right ventral occipital lobe selectively induced a significant shift to the right in the perceived midpoint for near- and far-space lines, respectively. The results reproduced in normal subjects the dissociation between neglect in near and far space that has been described in patients with different right-hemisphere lesions. This dissociation supports the contention that there is a dorsal/near space-ventral/far space segregation of processing in the visual system which reflects the behavioural goals of the two putative visual streams.
Transcranial magnetic stimulation (TMS) has been used to document some apparent interhemispheric influences behaviorally, with TMS over the right parietal cortex reported to enhance processing of touch for the ipsilateral right hand (Seyal et al., 1995). However, the neural bases of such apparent interhemispheric influences from TMS remain unknown. Here, we studied this directly by combining TMS with concurrent functional magnetic resonance imaging (fMRI). We applied bursts of 10 Hz TMS over right parietal cortex, at a high or low intensity, during two sensory contexts: either without any other stimulation, or while participants received median nerve stimulation to the right wrist, which projects to left primary somatosensory cortex (SI). TMS to right parietal cortex affected the blood oxygenation level-dependent signal in left SI, with high-versus low-intensity TMS increasing the left SI signal during right-wrist somatosensory input, but decreasing this in the absence of somatosensory input. This state-dependent modulation of SI by parietal TMS over the other hemisphere was accompanied by a related pattern of TMS-induced influences in the thalamus, as revealed by region-of-interest analyses. A behavioral experiment confirmed that the same right parietal TMS protocol of 10 Hz bursts led to enhanced detection of perithreshold electrical stimulation of the right median nerve, which is initially processed in left SI. Our results confirm directly that TMS over right parietal cortex can affect processing in left SI of the other hemisphere, with rivalrous effects (possibly transcallosal) arising in the absence of somatosensory input, but facilitatory effects (possibly involving thalamic circuitry) in the presence of driving somatosensory input.
We used concurrent TMS-fMRI to test directly for hemispheric differences in causal influences of right or left fronto-parietal cortex on activity (BOLD signal) in human occipital cortex. Clinical data and some behavioral TMS studies have been taken to suggest right-hemisphere specialization for top-down modulation of vision in humans, based on deficits such as spatial neglect or extinction in lesioned patients, or findings that TMS to right (versus left) fronto-parietal structures can elicit stronger effects on visual performance. But prior to the recent advent of concurrent TMS and neuroimaging, it was not possible to directly examine the causal impact of one (stimulated) brain region upon others in humans. Here we stimulated frontal or intraparietal cortex in the left or right hemisphere with TMS, inside an MR scanner, while measuring with fMRI any resulting BOLD signal changes in visual areas V1-V4 and V5/MT+. For both frontal and parietal stimulation, we found clear differences between effects of right-versus left-hemisphere TMS on activity in visual cortex, with all differences significant in direct statistical comparisons. Frontal TMS over either hemisphere elicited similar BOLD-decreases for central visual field representations in V1-V4, but only right frontal TMS led to BOLD-increases for peripheral field representations in these regions. Hemispheric differences for effects of parietal TMS were even more marked: Right parietal TMS led to strong BOLD changes in V1-V4 and V5/MT+, but left parietal TMS did not. These data directly confirm that human frontal and parietal cortex shows right-hemisphere specialization for causal influences on visual cortex.
Combining transcranial magnetic stimulation (TMS) with concurrent functional magnetic resonance imaging (fMRI) allows study of how local brain stimulation may causally affect activity in remote brain regions. Here, we applied bursts of high- or low-intensity TMS over right posterior parietal cortex, during a task requiring sustained covert visuospatial attention to either the left or right hemifield, or in a neutral control condition, while recording blood oxygenation-level–dependent signal with a posterior MR surface coil. As expected, the active attention conditions activated components of the well-described “attention network,” as compared with the neutral baseline. Also as expected, when comparing left minus right attention, or vice versa, contralateral occipital visual cortex was activated. The critical new finding was that the impact of high- minus low-intensity parietal TMS upon these visual regions depended on the currently attended side. High- minus low-intensity parietal TMS increased the difference between contralateral versus ipsilateral attention in right extrastriate visual cortex. A related albeit less pronounced pattern was found for left extrastriate visual cortex. Our results confirm that right human parietal cortex can exert attention-dependent influences on occipital visual cortex and provide a proof of concept for the use of concurrent TMS–fMRI in studying how remote influences can vary in a purely top–down manner with attentional demands.
We used concurrent transcranial magnetic stimulation and functional MRI (TMS-fMRI) during a visuospatial cueing paradigm in humans, to study the causal role of the right angular gyrus (AG) as a source of attentional control. Our findings show that TMS over the right AG (high vs. low intensity) modulates neural responses interhemispherically, in a manner that varies dynamically with the current attentional condition. The behavioural impact of such TMS depended not only on the target hemifield but also on exogenous cue validity, facilitating spatial reorienting to invalidly cued right visual targets. On a neural level, right AG TMS had corresponding interhemispheric effects in the left AG and left retinotopic cortex, including area V1. We conclude that the direction of covert visuospatial attention can involve dynamic interplay between the right AG and remote interconnected regions of the opposite left hemisphere, whereas our findings also suggest that the right AG can influence responses in the retinotopic visual cortex.
There is considerable inter-study and inter-individual variation in the scalp location of parietal sites where transcranial magnetic stimulation (TMS) may modulate visuospatial behaviours (see Ryan, Bonilha, & Jackson 2006); and no clear consensus on methods for identifying such sites. Here we introduce a novel TMS "hunting paradigm" that allows rapid, reliable identification of a site over right anterior intraparietal sulcus (IPS), where short trains (at 10 Hz for 0.5s) of TMS disrupt performance of a task in which subjects judge the presence or absence of a small peripheral gap (at 14 degrees eccentricity), on one or other (known) side of an extended (29 degrees) horizontal line centred on fixation. Signal detection analysis confirmed that TMS at this site reduced sensitivity (d') for gap targets in the left visual hemifield. A further experiment showed that the same right-parietal TMS increased sensitivity instead for gaps in the right hemifield. Comparing TMS across a grid of scalp locations around the identified 'hotspot' confirmed the spatial specificity. Assessment of the TMS intensity required to produce the phenomena found this was linearly related to individuals' resting motor TMS threshold over hand M1. Our approach provides a systematic new way to identify an effective site and intensity in individuals, at which TMS over right parietal cortex reliably changes visuospatial sensitivity.
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