Human dorsolateral prefrontal cortex is involved in visual search for conjunctions but not features: A theta TMS study

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.     

The role of the parietal cortex in visual attention--hemispheric asymmetries and the effects of learning: a magnetic stimulation study

Our previous studies of the role of the parietal cortex in visual learning and attention showed that the right parietal cortex is required for normal performance on conjunction visual search tasks but that its role depends on whether subjects are naive or trained on the task. Here we extend these findings in two Experiments. Experiment 1 shows that magnetic stimulation of the left parietal cortex also impairs performance (measured as reaction time) on conjunction visual search tasks, but only when the target is present in the right (contralateral) visual field. Stimulation of the same region on a feature detection task speeds up performance significantly when the target is in the left (ipsilateral) visual field. Experiment 2 explores further the role of the right parietal cortex in learning conjunction search tasks. Stimulation of the right parietal cortex in subjects who had already trained on some visual search tasks did not impair performance on a novel motion/form conjunction task even though the search was clearly serial. Stimulation of area V5, however, severely disrupted performance on the same task. These data indicate that the role of the parietal cortex may change much earlier in the course of training than initially thought.     

Frontal and parietal theta burst TMS impairs working memory for visual-spatial conjunctions

In tasks that selectively probe visual or spatial working memory (WM) frontal and posterior cortical areas show a segregation, with dorsal areas preferentially involved in spatial (e.g. location) WM and ventral areas in visual (e.g. object identity) WM. In a previous fMRI study [1], we showed that right parietal cortex (PC) was more active during WM for orientation, whereas left inferior frontal gyrus (IFG) was more active during colour WM. During WM for colour-orientation conjunctions, activity in these areas was intermediate to the level of activity for the single task preferred and non-preferred information. To examine whether these specialised areas play a critical role in coordinating visual and spatial WM to perform a conjunction task, we used theta burst transcranial magnetic stimulation (TMS) to induce a functional deficit. Compared to sham stimulation, TMS to right PC or left IFG selectively impaired WM for conjunctions but not single features. This is consistent with findings from visual search paradigms, in which frontal and parietal TMS selectively affects search for conjunctions compared to single features, and with combined TMS and functional imaging work suggesting that parietal and frontal regions are functionally coupled in tasks requiring integration of visual and spatial information. Our results thus elucidate mechanisms by which the brain coordinates spatially segregated processing streams and have implications beyond the field of working memory.     

Hemispheric differences in frontal and parietal influences on human occipital cortex: direct confirmation with concurrent TMS-fMRI

We used concurrent TMS-fMRI to test directly for hemispheric differences in causal influences of the right or left fronto-parietal cortex on activity (BOLD signal) in the 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 (vs. 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 the 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 the 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 the human frontal and parietal cortex show right-hemisphere specialization for causal influences on the visual cortex.     

The timing of the involvement of the frontal eye fields and posterior parietal cortex in visual search

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.     

Interhemispheric imbalance during visuospatial attention investigated by unilateral and bilateral TMS over human parietal cortices

We used single-pulse transcranial magnetic stimulation (TMS) to study visuospatial attention. TMS was applied over one hemisphere, or simultaneously over both the right and left posterior parietal cortex (PPC), at two different interstimulus intervals (ISI) during a visual detection task. Unilateral TMS over the right and left PPC, respectively, impaired detection of contralateral presented visual stimuli at an ISI of 150 ms. By contrast, simultaneous biparietal TMS induced no significant changes in correct stimulus detection. TMS at an ISI of 250 ms evoked no changes for magnetic stimulation over either the right or the left parietal cortex. These results suggest that both PPC play a crucial role at a relatively early stage in the widely distributed brain network of visuospatial attention. The abolition of behavioral deficits during simultaneous biparietal TMS underlines the common hypothesis that an interhemispheric imbalance might underlie the disorders of neglect and extinction seen following unilateral brain damage.     

Paired pulse TMS over the right posterior parietal cortex modulates visuospatial perception

OBJECTIVE: We previously observed a relative contralateral neglect by right parietal single-pulse TMS given 150 ms after visual stimulus presentation. Here we investigated the effects of parietal paired TMS in normal subjects performing a visuospatial task. METHODS: Thirteen right-handed healthy subjects underwent a line-length judgement task during single-pulse and paired (1, 3, 5, 10 ms ISIs) TMS, delivered on the right parietal cortex 150 ms after visual stimulus. RESULTS: Single pulse TMS over the right parietal cortex induced a significant rightward bias compared to the baseline condition. At 1 and 3 ms ISIs, paired-pulse TMS did not show any effect in comparison with single pulse TMS. More importantly, 5 ms ISI was able to restore baseline levels, thus inducing a significant improvement of the performance compared to single-pulse TMS and 1-3 ms ISIs. CONCLUSIONS: Paired TMS seems able to modulate activity of the right posterior parietal cortex in healthy subjects performing a cognitive visuospatial task.     

Temporal dynamics of parietal cortex involvement in visual search

The functional-neuroanatomic relationship that describes the involvement of the parietal cortex in visual search was investigated using repetitive transcranial magnetic stimulation (rTMS; 10 Hz, 500 ms in duration). Twelve adult participants performed feature-based visual search for a unique letter-without eye movements-under conditions that involved manipulations of search efficiency (efficient versus inefficient) and target-selection demands (set-size: 4 versus 10). rTMS was applied over the right posterior parietal cortex at the onset of the search array for all factorial conditions (0-500 ms); stimulation was additionally administered at 500 ms post-array onset (500-1000 ms) during inefficient search (set-size 10). Stimulation over the primary sensorimotor cortex served as a within-subjects control condition, and eye movements were monitored continuously. Significant increases in reaction time were restricted to parietal stimulation during inefficient search (set-size 10), with interference observed when rTMS was administered at the onset of the search array and at 500 ms post-array onset. The early effect was confined to target-present trials and the late effect was confined to target-absent trials, which may indicate temporally dissociable parietal involvement in target detection and response-based selection and/or search termination, respectively. Error rates did not vary significantly as a function of any of the independent variables. Taken together, these results are consistent with evidence from functional magnetic resonance studies indicating that inefficient feature-based visual search requires an intact parietal cortex, and also indicate that the parietal cortex is involved in inefficient search later than has been previously reported.     

Site-Dependent Effects of tDCS Uncover Dissociations in the Communication Network Underlying the Processing of Visual Search

BackgroundThe right posterior parietal cortex (rPPC) and the right frontal eye field (rFEF) form part of a network of brain areas involved in orienting spatial attention. Previous studies using transcranial magnetic stimulation (TMS) have demonstrated that both areas are critically involved in the processing of conjunction visual search tasks, since stimulation of these sites disrupts performance.ObjectiveThis study investigated the effects of long term neuronal modulation to rPPC and rFEF using transcranial direct current stimulation (tDCS) with the aim of uncovering sharing of these resources in the processing of conjunction visual search tasks.MethodsParticipants completed four blocks of conjunction search trials over the course of 45 min. Following the first block they received 15 min of either cathodal or anodal stimulation to rPPC or rFEF, or sham stimulation.ResultsA significant interaction between block and stimulation condition was found, indicating that tDCS caused different effects according to the site (rPPC or rFEF) and type of stimulation (cathodal, anodal, or sham). Practice resulted in a significant reduction in reaction time across the four blocks in all conditions except when cathodal tDCS was applied to rPPC.ConclusionsThe effects of cathodal tDCS over rPPC are subtler than those seen with TMS, and no effect of tDCS was evident at rFEF. This suggests that rFEF has a more transient role than rPPC in the processing of conjunction visual search and is robust to longer-term methods of neuro-disruption. Our results may be explained within the framework of functional connectivity between these, and other, areas.     

Maintenance of visual stability in the human posterior parietal cortex

Visual stability refers to our stable visuospatial perceptions despite the unstable visual input caused by saccades. Functional neuroimaging results, studies on patients with posterior parietal cortex (PPC) lesions, and single-unit recordings in the lateral intraparietal sulcus of primates indirectly suggest that the PPC might be a potential locus of visual stability through its involvement with spatial remapping. Here we directly explored the role of the PPC in visual stability by applying transcranial magnetic stimulation (TMS) while participants performed a perisaccadic displacement detection task. We show that TMS over the PPC but not a frontal control site alters sensitivity to displacement detection when administered just before contralateral saccades and that a general impairment in attention or in the perception of apparent motion cannot account for the decreased sensitivity. The specific relationship between the timing of TMS and saccade direction demonstrates that saccadic suppression of displacement (SSD) is likely a consequence of noisy contralateral spatial representations in the PPC around the time of a saccade. The same mechanism may keep the unstable visual world in the temporal proximity of saccades from reaching our consciousness.     

TMS over right posterior parietal cortex induces neglect in a scene-based frame of reference

Although damage to right posterior parietal cortex (RPPC) produces bias in line bisection, Karnath et al. [Karnath, H.-O., Berger, M. F., Küker, W., & Rorden, C. (2004). The anatomy of spatial neglect based on voxelwise statistical analysis: A study of 140 patients. Cerebral Cortex, 14, 1164-1172] claim that it plays little role in spatial neglect, which is better measured by target cancellation. We used a detection task (approximating cancellation in requiring detection) to investigate this claim by compromising the parietal cortex with transcranial magnetic stimulation (TMS). Two outline shapes, one on each side of fixation, were briefly displayed before a mask. The target was a discontinuity in the left or right of the outline of one of these perceptual objects. Subjects indicated position or absence of target as fast as possible. Stimulus-mask onset asynchrony was adjusted individually to yield 75% detection. TMS was delivered over left posterior parietal cortex (LPPC), RPPC and Vertex, with Sham TMS over RPPC as a baseline control. Target detection was near ceiling and fastest at central positions and worst and slowest at the far right. Detection was significantly reduced at the far left position by TMS over RPPC. No other effects were obtained and latency was not affected by TMS. Disruption of RPPC by TMS does produce left neglect as measured by detection. Given the pattern of performance and since it was disrupted on one side of the display rather than on one side of each shape, attention and neglect were in a scene-based rather than object-based reference frame.     

Reflexive and preparatory selection and suppression of salient information in the right and left posterior parietal cortex

Attentional cues can trigger activity in the parietal cortex in anticipation of visual displays, and this activity may, in turn, induce changes in other areas of the visual cortex, hence, implementing attentional selection. In a recent TMS study [Mevorach, C., Humphreys, G. W., & Shalev, L. Opposite biases in salience-based selection for the left and right posterior parietal cortex. Nature Neuroscience, 9, 740-742, 2006b], it was shown that the posterior parietal cortex (PPC) can utilize the relative saliency (a nonspatial property) of a target and a distractor to bias visual selection. Furthermore, selection was lateralized so that the right PPC is engaged when salient information must be selected and the left PPC when the salient information must be ignored. However, it is not clear how the PPC implements these complementary forms of selection. Here we used on-line triple-pulse TMS over the right or left PPC prior to or after the onset of global/local displays. When delivered after the onset of the display, TMS to the right PPC disrupted the selection of the more salient aspect of the hierarchical letter. In contrast, left PPC TMS delivered prior to the onset of the stimulus disrupted responses to the lower saliency stimulus. These findings suggest that selection and suppression of saliency, rather than being "two sides of the same coin," are fundamentally different processes. Selection of saliency seems to operate reflexively, whereas suppression of saliency relies on a preparatory phase that "sets up" the system in order to effectively ignore saliency.     

The role of the right superior temporal gyrus in visual search-insights from intraoperative electrical stimulation

Intraoperative electrical stimulation in awake patients is a seminal technique during brain surgery allowing one to infer the function of brain areas by temporary inactivation. Using this technique, we found that inactivation of the middle portion of the superior temporal gyrus (STG) leads to disturbed serial exploratory visual search. The data supplement recent findings by Ellison et al. [Ellison, A., Schindler, I., Pattison, L. L., & Milner, A. D. (2004). An exploration of the role of the superior temporal gyrus in visual search and spatial perception using TMS. Brain, 127, 2307-2315] using repetitive transcranial magnetic stimulation over the STG in healthy subjects. Our data demonstrate that the STG is integral to human exploration behaviour and challenge the traditional view that only the right posterior parietal cortex is involved in the mediation of visual search processes.     

The role of the left posterior parietal lobule in top-down modulation on space-based attention: a transcranial magnetic stimulation study

Converging evidence from neuroimaging as well as lesion and transcranial magnetic stimulation (TMS) studies has been obtained for the involvement of right ventral posterior parietal cortex (PPC) in exogenous orienting. However, the contribution of dorsal PPC to attentional orienting, particularly endogenous orienting, is still under debate. In an informative peripheral cueing paradigm, in which the exogenous and endogenous orienting can be studied in relative isolation within a single task, we applied TMS over sub-regions of dorsal PPC to explore their possible distinct involvement in exogenous and endogenous processes. We found that disruption of the left posterior intraparietal sulcus (pIPS) weakened the attentional effects of endogenous orienting, but did not affect exogenous processes. In addition, TMS applied over the right superior parietal lobule (SPL) resulted in an overall increase in reaction times. The present study provides the causal evidence that the left pIPS plays a crucial role in voluntary orienting of visual attention, while right SPL is involved in the processing of arousal and/or vigilance.     

Facilitation of bottom-up feature detection following rTMS-interference of the right parietal cortex

In visual search tasks the optimal strategy should utilize relevant information ignoring irrelevant one. When the information at the feature and object levels are in conflict, un-necessary processing at higher level of object shape can interfere with detection of lower level orientation feature.We explored the effects of inhibitory trains of transcranial magnetic stimulation (rTMS) on the right and left parietal cortex in healthy subjects performing two visual search tasks. One task (Task A) was characterised by an object-to-feature interference. The other task (Task B) was without such interference. We found that rTMS of the right parietal cortex significantly reduced reaction times (RTs) in Task A, where object recognition interferes with detection of orientation. This significant RT reduction was present only for the first 10 trials. Interestingly, right parietal rTMS had no effect on Task B. Moreover, rTMS of the left parietal cortex did not modify subjects’ RTs in either task. Subjects’ accuracy was equally affected by rTMS in both tasks over time.We suggest that inhibition of the right parietal cortex by means of rTMS facilitates feature-based visual search by inhibiting the interfering feature binding and spatial attentional processes. This allows subjects to accomplish Task A faster.     

TMS over posterior parietal cortex disrupts trans-saccadic visual stability

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.

Influence of monkey dorsolateral prefrontal and posterior parietal activity on behavioral choice during attention tasks

The dorsolateral prefrontal and the posterior parietal cortex have both been implicated in the guidance of visual attention. Traditionally, posterior parietal cortex has been thought to guide visual bottom‐up attention and prefrontal cortex to bias attention through top‐down information. More recent studies suggest a parallel time course of activation of the two areas in bottom‐up attention tasks, suggesting a common involvement, though these results do not necessarily imply identical roles. To address the specific roles of the two areas, we examined the influence of neuronal activity recorded from the prefrontal and parietal cortex of monkeys as they performed attention tasks based on choice probability and on correlation between reaction time and neuronal activity. The results revealed that posterior parietal but not dorsolateral prefrontal activity correlated with behavioral choice during the fixation period, prior to the appearance of the stimulus, resembling a bias factor. This preferential influence of posterior parietal activity on behavior was transient, so that dorsolateral prefrontal activity predicted choice after the appearance of the stimulus. Additionally, reaction time was better predicted by posterior parietal activity. These findings confirm the involvement of both dorsolateral prefrontal and posterior parietal cortex in the bottom‐up guidance of visual attention, but indicate different roles of the two areas in the guidance of attention and a dynamic time course of their effects, influencing behavior at different stages of the task.     

Signal-, set-, and movement-related activity in the human premotor cortex

Single unit recording studies in non-human premotor cortex have revealed neurons with motor-related activity. Other neurons, however, seem to be involved in prior movement selection and preparation processes, and have activity related to visual instruction signals or movement preparation ('set'). We have used single pulse transcranial magnetic stimulation (TMS) to identify similar processes in human subjects. In Experiment 1 subjects performed a cued movement task while being stimulated with TMS over three sites: sensorimotor cortex, posterior premotor cortex and anterior premotor cortex. TMS slowed movements when applied at 140 ms after the visual cue over the anterior premotor site, at 180 ms after the visual cue over the posterior premotor site, and at 220 ms and later after the visual cue over the sensorimotor cortex. The results are consistent with a change from signal to movement-related processing when moving from premotor to motor cortex. In Experiment 2 there was a preparatory set period between the instruction signal that informed subjects which movement to make and the 'go' signal that informed them when to actually make the movement. TMS was applied over the anterior premotor site and the sensorimotor site during the set period. At both sites TMS had similar effects on slowing subsequent movements. The results suggest set activity in both premotor and motor cortices in human subjects.     

Neural mechanisms of feature conjunction learning: Enduring changes in occipital cortex after a week of training

Most visual activities, whether reading, driving, or playing video games, require rapid detection and identification of learned patterns defined by arbitrary conjunctions of visual features. Initially, such detection is slow and inefficient, but it can become fast and efficient with training. To determine how the brain learns to process conjunctions of visual features efficiently, we trained participants over eight consecutive days to search for a target defined by an arbitrary conjunction of color and location among distractors with a different conjunction of the same features. During each training session, we measured brain activity with functional magnetic resonance imaging (fMRI). The speed of visual search for feature conjunctions improved dramatically within just a few days. These behavioral improvements were correlated with increased neural responses to the stimuli in visual cortex. This suggests that changes in neural processing in visual cortex contribute to the speeding up of visual feature conjunction search. We find evidence that this effect is driven by an increase in the signal‐to‐noise ratio (SNR) of the BOLD signal for search targets over distractors. In a control condition where target and distractor identities were exchanged after training, learned search efficiency was abolished, suggesting that the primary improvement was perceptual learning for the search stimuli, not task‐learning. Moreover, when participants were retested on the original task after nine months without further training, the acquired changes in behavior and brain activity were still present, showing that this can be an enduring form of learning and neural reorganization. Hum Brain Mapp 35:1201–1211, 2014. © 2013 Wiley Periodicals, Inc.     

Posterior parietal cortex mediates encoding and maintenance processes in change blindness

It is commonly accepted that right posterior parietal cortex (PPC) plays an important role in updating spatial representations, directing visuospatial attention, and planning actions. However, recent studies suggest that right PPC may also be involved in processes that are more closely associated with our visual awareness as its activation level positively correlates with successful conscious change detection (Beck, D.M., Rees, G., Frith, C.D., & Lavie, N. (2001). Neural correlates of change detection and change blindness. Nature Neuroscience, 4, 645-650.). Furthermore, disruption of its activity increases the occurrences of change blindness, thus suggesting a causal role for right PPC in change detection (Beck, D.M., Muggleton, N., Walsh, V., & Lavie, N. (2006). Right parietal cortex plays a critical role in change blindness. Cerebral Cortex, 16, 712-717.). In the context of a 1-shot change detection paradigm, we applied transcranial magnetic stimulation (TMS) during different time intervals to elucidate the temporally precise involvement of PPC in change detection. While subjects attempted to detect changes between two image sets separated by a brief time interval, TMS was applied either during the presentation of picture 1 when subjects were encoding and maintaining information into visual short-term memory, or picture 2 when subjects were retrieving information relating to picture 1 and comparing it to picture 2. Our results show that change blindness occurred more often when TMS was applied during the viewing of picture 1, which implies that right PPC plays a crucial role in the processes of encoding and maintaining information in visual short-term memory. In addition, since our stimuli did not involve changes in spatial locations, our findings also support previous studies suggesting that PPC may be involved in the processes of encoding non-spatial visual information (Todd, J.J. & Marois, R. (2004). Capacity limit of visual short-term memory in human posterior parietal cortex. Nature, 428, 751-754.).