The Behavioral Effects of tDCS on Visual Search Performance Are Not Influenced by the Location of the Reference Electrode.

We investigated the role of reference electrode placement (ipsilateral v contralateral frontal pole) on conjunction visual search task performance when the transcranial direct current stimulation (tDCS) cathode is placed over right posterior parietal cortex (rPPC) and over right frontal eye fields (rFEF), both of which have been shown to be causally involved in the processing of this task using TMS. This resulted in four experimental manipulations in which sham tDCS was applied in week one followed by active tDCS the following week. Another group received sham stimulation in both sessions to investigate practice effects over 1 week in this task. Results show that there is no difference between effects seen when the anode is placed ipsi or contralaterally. Cathodal stimulation of rPPC increased search times straight after stimulation similarly for ipsi and contralateral references. This finding does not extend to rFEF stimulation. However, for both sites and both montages, practice effects as seen in the sham/sham condition were negated. This can be taken as evidence that for this task, reference placement on either frontal pole is not important, but also that care needs to be taken when contextualizing tDCS "effects" that may not be immediately apparent particularly in between-participant designs.

Comparing the effect of temporal delay on the availability of egocentric and allocentric information in visual search.

Frames of reference play a central role in perceiving an object's location and reaching to pick that object up. It is thought that the ventral stream, believed to subserve vision for perception, utilises allocentric coding, while the dorsal stream, argued to be responsible for vision for action, primarily uses an egocentric reference frame. We have previously shown that egocentric representations can survive a delay; however, it is possible that in comparison to allocentric information, egocentric information decays more rapidly. Here we directly compare the effect of delay on the availability of egocentric and allocentric representations. We used spatial priming in visual search and repeated the location of the target relative to either a landmark in the search array (allocentric condition) or the observer's body (egocentric condition). Three inter-trial intervals created minimum delays between two consecutive trials of 2, 4, or 8seconds. In both conditions, search times to primed locations were faster than search times to un-primed locations. In the egocentric condition the effects were driven by a reduction in search times when egocentric information was repeated, an effect that was observed at all three delays. In the allocentric condition while search times did not change when the allocentric information was repeated, search times to un-primed target locations became slower. We conclude that egocentric representations are not as transient as previously thought but instead this information is still available, and can influence behaviour, after lengthy periods of delay. We also discuss the possible origins of the differences between allocentric and egocentric priming effects.

Reprint of: Object-based attentional facilitation and inhibition are neuropsychologically dissociated.

Salient peripheral cues produce a transient shift of attention which is superseded by a sustained inhibitory effect. Cueing part of an object produces an inhibitory cueing effect (ICE) that spreads throughout the object. In dynamic scenes the ICE stays with objects as they move. We examined object-centred attentional facilitation and inhibition in a patient with visual form agnosia. There was no evidence of object-centred attentional facilitation. In contrast, object-centred ICE was observed in 3 out of 4 tasks. These inhibitory effects were strongest where cues to objecthood were highly salient. These data are evidence of a neuropsychological dissociation between the facilitatory and inhibitory effects of attentional cueing. From a theoretical perspective the findings suggest that 'grouped arrays' are sufficient for object-based inhibition, but insufficient to generate object-centred attentional facilitation.

Object-based attentional facilitation and inhibition are neuropsychologically dissociated.

Salient peripheral cues produce a transient shift of attention which is superseded by a sustained inhibitory effect. Cueing part of an object produces an inhibitory cueing effect (ICE) that spreads throughout the object. In dynamic scenes the ICE stays with objects as they move. We examined object-centred attentional facilitation and inhibition in a patient with visual form agnosia. There was no evidence of object-centred attentional facilitation. In contrast, object-centred ICE was observed in 3 out of 4 tasks. These inhibitory effects were strongest where cues to objecthood were highly salient. These data are evidence of a neuropsychological dissociation between the facilitatory and inhibitory effects of attentional cueing. From a theoretical perspective the findings suggest that 'grouped arrays' are sufficient for object-based inhibition, but insufficient to generate object-centred attentional facilitation.

Dissociating the neural mechanisms of distance and spatial reference frames.

This study investigated if the neural mechanisms involved in processing distance (near and far) and frame of reference (egocentric and allocentric) can be dissociated. 36 participants completed a conjunction visual search task using either an egocentric (deciding if the target was to their left or right) or an allocentric (deciding if the target was to the left or right of a reference object) frame. Both tasks were performed in near (57 cm) and far (171 cm) space conditions. Participants were separated into three groups, and each received transcranial magnetic stimulation (TMS) to a different site; right posterior parietal cortex (rPPC), right ventral occipital cortex (rVO), or right frontal eye field (rFEF) in addition to sham TMS. The results show that rFEF is critical in the processing of each search at each distance whereas, contrary to previous detection results, TMS over rVO did not affect performance for any condition. TMS over rPPC revealed that specialised egocentric processing in the parietal cortex does not generalise to far space, providing evidence of a separation of the reference frame/distance conflation in the literature.

Oculomotor preparation as a rehearsal mechanism in spatial working memory.

There is little consensus regarding the specific processes responsible for encoding, maintenance, and retrieval of information in visuo-spatial working memory (VSWM). One influential theory is that VSWM may involve activation of the eye-movement (oculomotor) system. In this study we experimentally prevented healthy participants from planning or executing saccadic eye-movements during the encoding, maintenance, and retrieval stages of visual and spatial working memory tasks. Participants experienced a significant reduction in spatial memory span only when oculomotor preparation was prevented during encoding or maintenance. In contrast there was no reduction when oculomotor preparation was prevented only during retrieval. These results show that (a) involvement of the oculomotor system is necessary for optimal maintenance of directly-indicated locations in spatial working memory and (b) oculomotor preparation is not necessary during retrieval from spatial working memory. We propose that this study is the first to unambiguously demonstrate that the oculomotor system contributes to the maintenance of spatial locations in working memory independently from the involvement of covert attention.

The role of the oculomotor system in covert social attention.

Observing a change in gaze direction triggers a reflexive shift of attention and appears to engage the eye-movement system. However, the functional relationship between social attention and this oculomotor activation is unclear. One extremely influential hypothesis is that the preparation of a saccadic eye movement is necessary and sufficient for a covert, reflexive shift of attention (the premotor theory of attention; Rizzolatti et al., 1994). Surprisingly, this theory has not been directly tested with respect to reflexive gaze cueing. In order to address this issue, gaze cueing, peripheral cueing, and arrow cueing were examined under conditions in which some stimuli appeared at locations that could not become the goal of a saccadic eye movement. It was observed that peripheral cues failed to elicit reflexive attentional orienting when targets appeared beyond the range of eye movements. Similarly, nonpredictive arrow cues were ineffective when targets could not become the goal of a saccade. In contrast, significant gaze-cueing effects were still observed when targets were beyond the range of eye movements. These data demonstrate that the mechanisms involved in gaze cueing are dissociated from those involved in exogenous orienting to peripheral or arrow cues. Furthermore, the findings suggest that, unlike peripheral cueing and reflexive arrow cueing, gaze cueing is independent of oculomotor control. We conclude that the premotor theory does not offer a compelling explanation for gaze cueing.

Functional interaction between right parietal and bilateral frontal cortices during visual search tasks revealed using functional magnetic imaging and transcranial direct current stimulation.

The existence of a network of brain regions which are activated when one undertakes a difficult visual search task is well established. Two primary nodes on this network are right posterior parietal cortex (rPPC) and right frontal eye fields. Both have been shown to be involved in the orientation of attention, but the contingency that the activity of one of these areas has on the other is less clear. We sought to investigate this question by using transcranial direct current stimulation (tDCS) to selectively decrease activity in rPPC and then asking participants to perform a visual search task whilst undergoing functional magnetic resonance imaging. Comparison with a condition in which sham tDCS was applied revealed that cathodal tDCS over rPPC causes a selective bilateral decrease in frontal activity when performing a visual search task. This result demonstrates for the first time that premotor regions within the frontal lobe and rPPC are not only necessary to carry out a visual search task, but that they work together to bring about normal function.

Pointing in visual periphery: is DF's dorsal stream intact?

Observations of the visual form agnosic patient DF have been highly influential in establishing the hypothesis that separate processing streams deal with vision for perception (ventral stream) and vision for action (dorsal stream). In this context, DF's preserved ability to perform visually-guided actions has been contrasted with the selective impairment of visuomotor performance in optic ataxia patients suffering from damage to dorsal stream areas. However, the recent finding that DF shows a thinning of the grey matter in the dorsal stream regions of both hemispheres in combination with the observation that her right-handed movements are impaired when they are performed in visual periphery has opened up the possibility that patient DF may potentially also be suffering from optic ataxia. If lesions to the posterior parietal cortex (dorsal stream) are bilateral, pointing and reaching deficits should be observed in both visual hemifields and for both hands when targets are viewed in visual periphery. Here, we tested DF's visuomotor performance when pointing with her left and her right hand toward targets presented in the left and the right visual field at three different visual eccentricities. Our results indicate that DF shows large and consistent impairments in all conditions. These findings imply that DF's dorsal stream atrophies are functionally relevant and hence challenge the idea that patient DF's seemingly normal visuomotor behaviour can be attributed to her intact dorsal stream. Instead, DF seems to be a patient who suffers from combined ventral and dorsal stream damage meaning that a new account is needed to explain why she shows such remarkably normal visuomotor behaviour in a number of tasks and conditions.

Covert visual search within and beyond the effective oculomotor range.

Covert spatial attention is tightly coupled to the eye-movement system, but the precise nature of this coupling remains contentious. Recent research has argued that covert attention and overt eye-movements many share a common biological limit, such that covert exogenous orienting of attention is limited to stimuli that fall within the range of possible eye movements (the effective oculomotor range: EOMR). However, this conclusion is based on a single experimental paradigm: The Posner cueing task. Here, we examine the extent to which covert spatial attention is limited to the EOMR in visual search. Exogenous attention was assessed using a feature search task and endogenous attention assessed using a conjunction search task. The tasks were performed monocularly with the dominant eye in the frontal position or abducted by 40°. In the abducted position stimuli in the temporal hemispace could be seen, but could not become the goal of a saccadic eye-movement (i.e. they were beyond the EOMR). In contrast, stimuli in the nasal hemifield remained within the EOMR. We observed a significant effect of eye-abduction on feature search, such that search was slower when targets appeared beyond the EOMR. In contrast, eye-abduction had no effect on search times during conjunction search. Set size did not interact with target location or eye-position. It is concluded that optimal covert orienting of exogenous attention in visual search is restricted to locations within the effective oculomotor range.

Oculomotor involvement in spatial working memory is task-specific.

Many everyday tasks, such as remembering where you parked, require the capacity to store and manipulate information about the visual and spatial properties of the world. The ability to represent, remember, and manipulate spatial information is known as visuospatial working memory (VSWM). Despite substantial interest in VSWM the mechanisms responsible for this ability remain debated. One influential idea is that VSWM depends on activity in the eye-movement (oculomotor) system. However, this has proved difficult to test because experimental paradigms that disrupt oculomotor control also interfere with other cognitive systems, such as spatial attention. Here, we present data from a novel paradigm that selectively disrupts activation in the oculomotor system. We show that the inability to make eye-movements is associated with impaired performance on the Corsi Blocks task, but not on Arrow Span, Visual Patterns, Size Estimation or Digit Span tasks. It is argued that the oculomotor system is required to encode and maintain spatial locations indicted by a change in physical salience, but not non-salient spatial locations indicated by the meaning of a symbolic cue. This suggestion offers a way to reconcile the currently conflicting evidence regarding the role of the oculomotor system in spatial working memory.

Site-dependent effects of tDCS uncover dissociations in the communication network underlying the processing of visual search.

BACKGROUND: The 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. OBJECTIVE: This 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. METHODS: Participants 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. RESULTS: A 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. CONCLUSIONS: The 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.

Near and far space: Understanding the neural mechanisms of spatial attention.

Visuospatial neglect is a multicomponent syndrome, and one dissociation reported is between neglect for near (peripersonal) and far (extrapersonal) space. Owing to patient heterogeneity and extensive lesions, it is difficult to determine the precise neural mechanisms underlying this dissociation using clinical methodology. In this study, transcranial magnetic stimulation was used to examine the involvement of three areas in the undamaged brain, while participants completed a conjunction search task in near and far space. The brain areas investigated were right posterior parietal cortex (rPPC), right frontal eye field (rFEF), and right ventral occipital cortex (rVO), each of which has been implicated in visuospatial processing. The results revealed a double dissociation, whereby rPPC was involved for search in near space only, whilst rVO only became necessary when the task was completed in far space. These data provide clear evidence for a dorsal and ventral dissociation between the processing of near and far space, which is compatible with the functional roles previously attributed to the two streams. For example, the involvement of the dorsal stream in near space reflects its role in vision for action, because it is within this spatial location that actions can be performed. The results also revealed that rFEF is involved in the processing of visual search in both near and far space and may contribute to visuospatial attention and/or the control of eye-movements irrespective of spatial frame. We discuss our results with respect to their clear ramifications for clinical diagnosis and neurorehabilitation.

Inhibition of return impairs phosphene detection.

Efficient visual exploration requires the ability to select possible target locations via spatial attention and to deselect previously inspected locations via inhibition of return (IOR). Although a great deal is known about the effects of spatial attention on processing in visual cortex, much less is known about the effects of IOR on early visual areas. One possibility is that IOR acts in an opposite way to spatial attention, such that, whereas spatial attention enhances target related neural signals in visual cortex, IOR suppress target-related signals. Using a novel dual-coil TMS protocol, we found that IOR reduced the probability of detecting a TMS-induced phosphene in extrastriate cortex (V5). Specifically, a nonpredictive spatial precue presented 500 or 800 msec before stimulation significantly reduced the probability of detecting a phosphene when the precue appeared contralaterally to the site of stimulation (i.e., ipsilaterally to the potential location of the phosphene), compared with ipsilaterally or centrally presented cues. This result demonstrates that IOR facilitates visual exploration by directly affecting the strength of target-related signals in extrastriate visual cortex. This result is consistent with neurophysiological models of attention, which postulate that IOR modulates perception by biasing competition between sensory representations.

Visuomotor performance based on peripheral vision is impaired in the visual form agnostic patient DF.

The perception-action model states that visual information is processed in different cortical areas depending on the purpose for which the information is acquired. Specifically, it was suggested that the ventral stream mediates visual perception, whereas the dorsal stream primarily processes visual information for the guidance of actions (Goodale & Milner, 1992). Evidence for the model comes from patient studies showing that patients with ventral stream damage (visual form agnosia) and patients with dorsal stream damage (optic ataxia) show divergent performance in action and perception tasks. Whereas DF, a patient suffering from visual form agnosia, was found to perform well in visuomotor tasks despite her inability to use vision for perceptual tasks, patients with optic ataxia show usually the opposite pattern, i.e. good perception but impaired visuomotor control. The finding that both disorders seem to provoke a mirror-reversed pattern of spared and impaired visual functions, led to the belief that optic ataxia and visual form agnosia can be considered as complementary disorders. However, the visuomotor performance of patients with optic ataxia is typically only impaired when they are tested in visual periphery while being often preserved when tested in central vision. Here, we show that DF's visuomotor performance is also only preserved when the target is presented centrally. Her reaching and grasping movements to targets in peripheral vision are abnormal. Our findings indicate that DF's visuomotor performance is quite similar to the visuomotor performance of patients with optic ataxia which undermines previous suggestions that the two disorders form a double-dissociation.

Spatial priming in visual search: memory for body-centred information.

Spatial priming allows memory for target locations to be evaluated, whereby when a target appears in the same location across trials, participants become more efficient at locating it and consequently their search times decrease. Previously, we reported priming effects when the location of a target was repeated with respect to the participant's body but not when it was repeated relative to their eye position; therefore, suggesting that body-centred information is available after a delay of at least a few seconds (Ball et al. in Exp Brain Res 204:585-594, 2010). However, we were unable to rule out the possibility that stable allocentric cues within the room may have contributed to the priming effects that we observed. In this current study, we introduced a condition where despite participants moving to a new location between trials, their position relative to the target was maintained. This movement disrupted any potential room-based cues about the target location. While we replicated our previous finding of priming when the location of the target was repeated relative to the viewer when no movement was required, we also found robust priming effects when participants moved to a new location in between trials. Thus, we provide clear evidence that in our spatial priming task, the location of the target was being coded in a body-centred reference frame and that this information is available after a delay.

A body-centred frame of reference drives spatial priming in visual search.

Spatial priming in visual search is a well-documented phenomenon. If the target of a visual search is presented at the same location in subsequent trials, the time taken to find the target at this repeated target location is significantly reduced. Previous studies did not determine which spatial reference frame is used to code the location. At least two reference frames can be distinguished: an observer-related frame of reference (egocentric) or a scene-based frame of reference (allocentric). While past studies suggest that an allocentric reference frame is more effective, we found that an egocentric reference frame is at least as effective as an allocentric one (Ball et al. Neuropsychologia 47(6):1585-1591, 2009). Our previous study did not identify which specific egocentric reference frame was used for the priming: participants could have used a retinotopic or a body-centred frame of reference. Here, we disentangled the retinotopic and body-centred reference frames. In the retinotopic condition, the position of the target stimulus, when repeated, changed with the fixation position, whereas in the body-centred condition, the position of the target stimulus remained the same relative to the display, and thus to the body-midline, but was different relative to the fixation position. We used a conjunction search task to assess the generality of our previous findings. We found that participants relied on body-centred information and not retinotopic cues. Thus, we provide further evidence that egocentric information, and specifically body-centred information, can persist for several seconds, and that these effects are not specific to either a feature or a conjunction search paradigm.

Deficits of reflexive attention induced by abduction of the eye.

Attention mediates access of sensory events to higher cognitive systems and can be driven by either top-down voluntary mechanisms or in a bottom-up, reflexive fashion by the sensory properties of a stimulus. The exact mechanisms underlying these different modes of attention are controversial, but both types of attention appear to be tightly coupled to the systems used for the control of eye-movements. Indeed, recent data indicates that patients with opthalmoplegia (paralysis of the eyes) have difficulty voluntarily attending to locations to which saccades cannot be made (Craighero, Carta, & Fadiga, 2001) and experimentally induced opthalmoplegia disrupts voluntary attention in normal participants. However, the extent to which reflexive attention is mediated by the ability to make eye-movements in normal participants remains unclear. Here, we address this issue by investigating the effect of an experimentally induced opthalmoplegia on voluntary and reflexive attentional orienting during visual search. We observed that abducting the eye into the temporal hemifield elicited deficits of both voluntary and reflexive attention for targets that appeared beyond the oculomotor range. This result confirms the link between oculomotor control and voluntary attention observed in opthalmoplegic patients and demonstrates for the first time that reflexive attention is mediated by the ability to make eye-movements in normal participants.

Both egocentric and allocentric cues support spatial priming in visual search.

The perception-action model proposes that vision for perception and vision for action are subserved by two separate cortical systems, the ventral and dorsal streams, respectively [Milner, A. D., & Goodale, M. A. (1995). The visual brain in action (1st ed.). Oxford: Oxford University Press; Milner, A. D., & Goodale, M. A. (2006). The visual brain in action (2nd ed.). Oxford: Oxford University Press Inc.]. The dorsal stream codes spatial information egocentrically, that is, relative to the observer. Egocentric representations are argued to be highly transient; therefore, it might be expected that egocentric information cannot be used for spatial memory tasks, even when the visual information only needs to be retained for a few seconds. Here, by applying a spatial priming paradigm to a visual search task, we investigated whether short-term spatial memory can use egocentric information. Spatial priming manifests itself in speeded detection times for a target when that target appears in the same location it previously appeared in. Target locations can be defined in either egocentric or allocentric (i.e. relative to other items in the display) frames of reference; however, it is unclear which of these are used in spatial priming, or if both are. Our results show that both allocentric and egocentric cues were used in spatial priming, and that egocentric cues were in fact more effective than allocentric cues for short-term priming. We conclude that egocentric information can persist for several seconds; a conclusion which is at odds with the assumption of the perception-action model that egocentric representations are highly transient.