Disruption of reflexive attention and eye movements in an individual with a collicular lesion

The superior colliculus (SC) plays a central role in the control of saccadic eye movements and has also been implicated in control of covert spatial attention. While there is a growing body of evidence from studies of awake behaving primates that supports these proposals, direct evidence from humans has been sparse. In the present study we tested a patient with thiamine deficiency and a lesion of the SC, who performed both eye movement tasks (prosaccades and antisaccades, with or without a gap) and a covert spatial attention task assessing inhibition of return (IOR). For eye movements, the gap effect was disrupted, and abnormal saccade metrics occurred, with reflexive eye movements being disrupted moreso than voluntary eye movements. Each of these effects resolved coincident with thiamine treatment. The covert attention task revealed a complete absence of IOR. The unequal disruption of voluntary and reflexive eye movements supports the idea that oculomotor responses can be generated in an independent fashion by frontal cortical and lower level neural systems. The role of the SC and other structures in these orienting processes is discussed.     

Ocular motor ability and covert attention in patients with Duane Retraction Syndrome

Is orienting of spatial attention dependent on normal functioning of the ocular motor system? We investigated the role of motor pathways in covert orienting (attentional orienting without performing eye movements) by studying three patients suffering from Duane Retraction Syndrome—a congenital impairment in executing horizontal eye movements restricted to specific gaze directions. Patients showed a typical exogenous (reflexive) attention effect when the target was presented in visual fields to which they could perform an eye movement. This effect was not present when the target was presented in the visual field to which they could not perform eye movements. These findings stress the link between eye movements and attention. Specifically, they bring out the importance of the ability to execute appropriate eye movements for attentional orienting. We suggest that the relevant information about eye movement ability is provided by feedback from lower motor structures to higher attentional areas.     

Covert reorienting and inhibition of return: an event-related fMRI study

Using event-related fMRI, we analyzed the functional neuroanatomy of covert reorienting and inhibition of return (IOR). Covert reorienting to a target appearing within 250 msec after an invalid contralateral location cue elicited increased activation in the left fronto-polar cortex (LFPC), right anterior and left posterior middle frontal gyrus, and right cerebellum, areas that have previously been associated with attentional processes, specifically attentional change. In contrast, IOR, which leads to prolonged response times to targets that appear at the cued location at a stimulus-onset-asynchrony (SOA)>250 msec, was accompanied by increased activation in brain areas involved in oculomotor programming, such as the right medial frontal gyrus (supplementary eye field; SEF) and the right inferior precentral sulcus (frontal eye field; FEF), supporting the oculomotor bias theory of IOR. Pre-SEF and pre-FEF areas were involved both in covert reorienting and IOR. The supramarginal gyri were bilaterally involved in IOR, with the right supramarginal gyrus additionally involved in covert reorienting.     

Neural correlates of covert orienting of visual spatial attention along vertical and horizontal dimensions

Covert orienting of spatial attention along the horizontal meridian of the visual field is mediated by a fronto-parietal neural network. The neural substrates underlying covert orienting of attention along the vertical meridian, however, are less understood. We recorded hemodynamic responses using functional magnetic resonance imaging (fMRI) from healthy volunteers in covert visual orienting tasks that required to detect targets either at the fixation or at peripheral attended locations on the horizontal or vertical meridian in the left (LVF), right (RVF), upper (UVF), and lower (LoVF) visual fields. We found that, relative to when attention was at the fixation, covert orienting of attention along the horizontal and vertical meridia induced enhanced activities in the superior parietal and frontal lobes bilaterally and the cerebellum. In addition, attention to the LoVF and UVF generated stronger activation in the medial frontal cortex, anterior cingulate, precuneus, and the cerebellum relative to attention along the horizontal meridian. The reversed contrast, however, produced stronger activation in the right lingual gyrus and right premotor cortex. The fMRI results suggest that, while a common neural network is engaged in guiding visual spatial attention along the vertical and horizontal dimensions, unique neural correlates are associated with covert attentional orienting along the vertical and horizontal meridia of the visual field.     

Attention and sensory interactions within the occipital cortex in the early blind: an fMRI study

Visual deprivation early in life results in occipital cortical responsiveness across a broad range of perceptual and cognitive tasks. In the reorganized occipital cortex of early blind (EB) individuals, the relative lack of specificity for particular sensory stimuli and tasks suggests that attention effects may play a prominent role in these areas. We wished to establish whether occipital cortical areas in the EB were responsive to stimuli across sensory modalities (auditory, tactile) and whether these areas maintained or altered their activity as a function of selective attention. Using a three-stimulus oddball paradigm and event-related functional magnetic resonance imaging, auditory and tactile tasks presented separately demonstrated that several occipital regions of interest (ROIs) in the EB, but not sighted controls (SCs), responded to targets and task-irrelevant distracter stimuli of both modalities. When auditory and tactile stimuli were presented simultaneously with subjects alternating attention between sensory streams, only the calcarine sulcus continued to respond to stimuli in both modalities. In all other ROIs, responses to auditory targets were as large or larger than those observed in the auditory-alone condition, but responses to tactile targets were attenuated or abolished by the presence of unattended auditory stimuli. Both auditory and somatosensory cortices responded consistently to auditory and tactile targets, respectively. These results reveal mechanisms of orienting and selective attention within the visual cortex of EB individuals and suggest that mechanisms of enhancement and suppression interact asymmetrically on auditory and tactile streams during bimodal sensory presentation.     

Deconstructing the architecture of dorsal and ventral attention systems with dynamic causal modeling

Attentional orientation to a spatial cue and reorientation-after invalid cueing-are mediated by two distinct networks in the human brain. A bilateral dorsal frontoparietal network, comprising the intraparietal sulcus (IPS) and the frontal eye fields (FEF), controls the voluntary deployment of attention and may modulate visual cortex in preparation for upcoming stimulation. In contrast, reorienting attention to invalidly cued targets engages a right-lateralized ventral frontoparietal network comprising the temporoparietal junction (TPJ) and ventral frontal cortex. The present fMRI study investigated the functional architecture of these two attentional systems by characterizing effective connectivity during lateralized orienting and reorienting of attention, respectively. Subjects performed a modified version of Posner's location-cueing paradigm. Dynamic causal modeling (DCM) of regional responses in the dorsal and ventral network, identified in a conventional (SPM) whole-brain analysis, was used to compare different functional architectures. Bayesian model selection showed that top-down connections from left and right IPS to left and right visual cortex, respectively, were modulated by the direction of attention. Moreover, model evidence was highest for a model with directed influences from bilateral IPS to FEF, and reciprocal coupling between right and left FEF. Invalid cueing enhanced forward connections from visual areas to right TPJ, and directed influences from right TPJ to right IPS and IFG (inferior frontal gyrus). These findings shed further light on the functional organization of the dorsal and ventral attentional network and support a context-sensitive lateralization in the top-down (backward) mediation of attentional orienting and the bottom-up (forward) effects of invalid cueing.     

Spatial auditory compensation in early-blind humans: involvement of eye movements and/or attention orienting?

Several studies have reported that the early-blind displays higher auditory spatial abilities than the sighted. Although many studies have attempted to delineate the cortical structures that undergo functional reorganization in blind people, few have tried to determine which auditory or non-auditory processes mediate these increased auditory spatial abilities. The aim of this paper is to investigate the role of eye movements and orientation of attention in auditory localization in blind humans. Although we found, in a first experiment, that the influence of eye movements on auditory spatial localization is preserved in spite of congenital visual deprivation, the saccade influence on spatial hearing is not more pronounced in the blind than in the sighted. In a second experiment, early-blind and sighted subjects undertook a task involving discrimination of sound elevation in which auditory targets followed uninformative auditory cues on either side with an intermediate elevation. When sounds were emitted from the frontal hemifield, both groups showed similar auditory localization performance. Although the auditory cue did not affect discrimination accuracy in both groups, early-blind subjects exhibited shorter reaction times than sighted subjects when sound sources were placed at far-lateral locations. Attentional cues, however, had similar effects on both groups of subjects, suggesting that improved auditory spatial abilities are not mediated by attention orienting mechanisms.     

ERP correlates of shared control mechanisms involved in saccade preparation and in covert attention

We investigated whether attention shifts and eye movement preparation are mediated by shared control mechanisms, as claimed by the premotor theory of attention. ERPs were recorded in three tasks where directional cues presented at the beginning of each trial instructed participants to direct their attention to the cued side without eye movements (Covert task), to prepare an eye movement in the cued direction without attention shifts (Saccade task) or both (Combined task). A peripheral visual Go/Nogo stimulus that was presented 800 ms after cue onset signalled whether responses had to be executed or withheld. Lateralised ERP components triggered during the cue-target interval, which are assumed to reflect preparatory control mechanisms that mediate attentional orienting, were very similar across tasks. They were also present in the Saccade task, which was designed to discourage any concomitant covert attention shifts. These results support the hypothesis that saccade preparation and attentional orienting are implemented by common control structures. There were however systematic differences in the impact of eye movement programming and covert attention on ERPs triggered in response to visual stimuli at cued versus uncued locations. It is concluded that, although the preparatory processes underlying saccade programming and covert attentional orienting may be based on common mechanisms, they nevertheless differ in their spatially specific effects on visual information processing.     

Covert and overt voluntary attention: linked or independent?

Recent evidence indicates that reflexive shifts in spatial attention with eye movements (overt orienting) and without eye movements (covert orienting) can be dissociated [J. Exp. Psychol. Hum. Percept. Perform., in press]. Here, we show that a similar dissociation exists for voluntary shifts in overt and covert attention. Our study is consistent with general theories of attention that assume bottom-up (reflexive) processes and top-down (voluntary) processes converge on a common neural architecture.     

Cortical activation patterns during voluntary blinks and voluntary saccades

OBJECTIVE: To investigate the activation of frontal, parietal, and occipital areas in normal volunteers during voluntary blinks and during voluntary saccades using functional MRI (fMRI). BACKGROUND: A previous fMRI study revealed the activation of the precentral and posterior middle frontal gyrus ("frontal eye field" [FEF]), the medial part of the superior frontal gyrus ("supplementary eye field" [SEF]), and the visual cortex. The parietal cortex was not included in this study. Frontal and occipital cortical areas involved in voluntary blinking have not been shown previously using fMRI. METHODS: A 1.5-T standard clinical scanner was used for both anatomic and functional studies in 12 observers. To conduct data analyses the authors used voxel-by-voxel cross-correlation. RESULTS: Voluntary blinks led to the activation (p < 0.05) of the FEF, the SEF, the posterior parietal cortex ("parietal eye field" [PEF]), and the visual cortex. Voluntary blinking produced activity in the same cerebral structures as voluntary saccades. However, the number of activated voxels was smaller during voluntary blinking than during voluntary saccades in the visual cortex and in the FEF (p < 0.01). In contrast, the extent of activation was significantly higher (p < 0.003) in the SEF and in the PEF during voluntary blinking. CONCLUSIONS: Voluntary blinks and saccades are associated with similar loci of activation patterns; however, the quantitative distribution of activation suggests that the middle part of the frontal gyrus and posterior parietal cortex are of special significance for voluntary blinks. The results argue for the importance of considering quantitative distributional properties of parallel cortical activities associated with saccades and blinks.     

Brain responses to biological relevance

This study examines whether orienting attention to biologically based social cues engages neural mechanisms distinct from those engaged by orienting to nonbiologically based nonsocial cues. Participants viewed a perceptually ambiguous stimulus presented centrally while performing a target detection task. By having participants alternate between viewing this stimulus as an eye in profile or an arrowhead, we were able to directly compare the neural mechanisms of attentional orienting to social and nonsocial cues while holding the physical stimulus constant. The functional magnetic resonance imaging results indicated that attentional orienting to both eye gaze and arrow cues engaged extensive dorsal and ventral fronto-parietal networks. Eye gaze cues, however, more vigorously engaged two regions in the ventral frontal cortex associated with attentional reorienting to salient or meaningful stimuli, as well as lateral occipital regions. An event-related potential study demonstrated that this enhanced occipital response was attributable to a higher-amplitude sensory gain effect for targets appearing at locations cued by eye gaze than for those cued by an arrowhead. These results endorse the hypothesis that differences in attention to social and nonsocial cues are quantitative rather than qualitative, running counter to current models that assume enhanced processing for social stimuli reflects the involvement of a unique network of brain regions. An intriguing implication of the present study is the possibility that our ability to orient volitionally and reflexively to socially irrelevant stimuli, including arrowheads, may have arisen as a useful by-product of a system that developed first, and foremost, to promote social orienting to stimuli that are biologically relevant.     

An event‐related FMRI study of exogenous orienting across vision and audition

The orienting of attention to the spatial location of sensory stimuli in one modality based on sensory stimuli presented in another modality (i.e., cross‐modal orienting) is a common mechanism for controlling attentional shifts. The neuronal mechanisms of top‐down cross‐modal orienting have been studied extensively. However, the neuronal substrates of bottom‐up audio‐visual cross‐modal spatial orienting remain to be elucidated. Therefore, behavioral and event‐related functional magnetic resonance imaging (FMRI) data were collected while healthy volunteers (N = 26) performed a spatial cross‐modal localization task modeled after the Posner cuing paradigm. Behavioral results indicated that although both visual and auditory cues were effective in producing bottom‐up shifts of cross‐modal spatial attention, reorienting effects were greater for the visual cues condition. Statistically significant evidence of inhibition of return was not observed for either condition. Functional results also indicated that visual cues with auditory targets resulted in greater activation within ventral and dorsal frontoparietal attention networks, visual and auditory “where” streams, primary auditory cortex, and thalamus during reorienting across both short and long stimulus onset asynchronys. In contrast, no areas of unique activation were associated with reorienting following auditory cues with visual targets. In summary, current results question whether audio‐visual cross‐modal orienting is supramodal in nature, suggesting rather that the initial modality of cue presentation heavily influences both behavioral and functional results. In the context of localization tasks, reorienting effects accompanied by the activation of the frontoparietal reorienting network are more robust for visual cues with auditory targets than for auditory cues with visual targets. Hum Brain Mapp 35:964–974, 2014. © 2013 Wiley Periodicals, Inc.     

Anterior intraparietal sulcus is sensitive to bottom-up attention driven by stimulus salience

Frontal eye fields (FEF) and anterior intraparietal sulcus (aIPS) are involved in the control of voluntary attention in humans, but their functional differences remain poorly understood. We examined the activity in these brain regions as a function of task-irrelevant changes in target and nontarget perceptual salience during a sustained spatial attention task. Both aIPS and FEF were engaged during selective attention. FEF, but not aIPS, was sensitive to the direction of spatial attention. Conversely, aIPS, but not FEF, was modulated by the relative perceptual salience of the target and nontarget stimuli. These results demonstrate separable roles for FEF and aIPS in attentional control with FEF more involved in goal-directed spatial attention and aIPS relatively more sensitive to bottom-up attentional influences driven by stimulus salience.     

Prepare for conflict: EEG correlates of the anticipation of target competition during overt and covert shifts of visual attention

When preparing to make a saccadic eye movement in a cued direction, perception of stimuli at the target location is enhanced, just as it is when attention is covertly deployed there. Accordingly, the timing and anatomical sources of preparatory brain activity accompanying shifts of covert attention and saccade preparation tend to exhibit a large degree of overlap. However, there is evidence that preparatory processes are modulated by the foreknowledge of visual distractor competition during covert attention, and it is unknown whether eye movement preparation undergoes equivalent modulation. Here we examine preparatory processes in the electroencephalogram of human participants during four blocked versions of a spatial cueing task, requiring either covert detection or saccade execution, and either containing a distractor or not. As in previous work, a typical pattern of spatially selective occipital, parietal and frontal activity was seen in all task versions. However, whereas distractor presence called on an enhancement of spatially selective visual cortical modulation during covert attention, it instead called on increased activity over frontomedial oculomotor areas in the case of overt saccade preparation. We conclude that, although advance orienting signals may be similar in character during overt and covert conditions, the pattern by which these signals are modulated to ameliorate the behavioral costs of distractor competition is highly distinct, pointing to a degree of separability between the overt and covert systems.     

Spatial and nonspatial peripheral auditory processing in congenitally blind people

Congenitally blind adults' performance in spatial and nonspatial peripheral auditory attention tasks was compared with that of sighted adults in a paradigm manipulating location-based and frequency-based inhibition of return concurrently. Blind study participants responded faster in spatial attention tasks (detection/localization) and slower in the nonspatial frequency discrimination task than sighted participants. Both groups, however, showed the same patterns of interaction between location-based and frequency-based inhibition of return. These results suggest that early vision deprivation enhances the function of the posterior-dorsal auditory 'where' pathway but impairs the function of the anterior-ventral 'what' pathway during peripheral auditory attention. The altered processing speed in the blind, however, is not accompanied by alteration in attentional orienting mechanisms that may be localized to higher cortices.     

Spatial orienting in complex audiovisual environments

Previous studies on crossmodal spatial orienting typically used simple and stereotyped stimuli in the absence of any meaningful context. This study combined computational models, behavioural measures and functional magnetic resonance imaging to investigate audiovisual spatial interactions in naturalistic settings. We created short videos portraying everyday life situations that included a lateralised visual event and a co‐occurring sound, either on the same or on the opposite side of space. Subjects viewed the videos with or without eye‐movements allowed (overt or covert orienting). For each video, visual and auditory saliency maps were used to index the strength of stimulus‐driven signals, and eye‐movements were used as a measure of the efficacy of the audiovisual events for spatial orienting. Results showed that visual salience modulated activity in higher‐order visual areas, whereas auditory salience modulated activity in the superior temporal cortex. Auditory salience modulated activity also in the posterior parietal cortex, but only when audiovisual stimuli occurred on the same side of space (multisensory spatial congruence). Orienting efficacy affected activity in the visual cortex, within the same regions modulated by visual salience. These patterns of activation were comparable in overt and covert orienting conditions. Our results demonstrate that, during viewing of complex multisensory stimuli, activity in sensory areas reflects both stimulus‐driven signals and their efficacy for spatial orienting; and that the posterior parietal cortex combines spatial information about the visual and the auditory modality. Hum Brain Mapp 35:1597–1614, 2014. © 2013 Wiley Periodicals, Inc.     

Dynamic activation of frontal, parietal, and sensory regions underlying anticipatory visual spatial attention

Although it is well established that multiple frontal, parietal, and occipital regions in humans are involved in anticipatory deployment of visual spatial attention, less is known about the electrophysiological signals in each region across multiple subsecond periods of attentional deployment. We used MEG measures of cortical stimulus-locked, signal-averaged (event-related field) activity during a task in which a symbolic cue directed covert attention to the relevant location on each trial. Direction-specific attention effects occurred in different cortical regions for each of multiple time periods during the delay between the cue and imperative stimulus. A sequence of activation from V1/V2 to extrastriate, parietal, and frontal regions occurred within 110 ms after cue, possibly related to extraction of cue meaning. Direction-specific activations ～300 ms after cue in frontal eye field (FEF), lateral intraparietal area (LIP), and cuneus support early covert targeting of the cued location. This was followed by coactivation of a frontal-parietal system [superior frontal gyrus (SFG), middle frontal gyrus (MFG), LIP, anterior intraparietal sulcus (IPSa)] that may coordinate the transition from targeting the cued location to sustained deployment of attention to both space and feature in the last period. The last period involved direction-specific activity in parietal regions and both dorsal and ventral sensory regions [LIP, IPSa, ventral IPS, lateral occipital region, and fusiform gyrus], which was accompanied by activation that was not direction specific in right hemisphere frontal regions (FEF, SFG, MFG). Behavioral performance corresponded with the magnitude of attention-related activity in different brain regions at each time period during deployment. The results add to the emerging electrophysiological characterization of different cortical networks that operate during anticipatory deployment of visual spatial attention.     

Ventral and dorsal visual pathways support auditory motion processing in the blind: evidence from electrical neuroimaging

Blindness induces processes of neural plasticity, resulting in recruitment of the deafferentated visual areas for non‐visual sensory functions. These processes are related to superior abilities of blind compared with sighted individuals for specific auditory and tactile tasks. Recently, an exceptional performance of the blind has been demonstrated for auditory motion perception, with a minimum audible movement angle that was half that of sighted controls (J. Lewald (2013) Neuropsychologia, 51 , 181–186). The present study revealed an electrophysiological correlate of this finding by analysing the so‐called motion‐onset response, a prominent auditory‐evoked potential to the onset of motion. The cN1 component of this response, appearing about 170 ms after motion onset, was two times higher in amplitude for blind compared with matched sighted control subjects. At the time of the cN1, electrical neuroimaging using sLORETA revealed stronger activation in blind than sighted subjects primarily in ventral visual areas (V1v, V2v, VP, V4v) of the right occipital lobe. Activation was also obtained in middle temporal area V5. These findings suggest that blindness results in stronger involvement of both non‐motion areas of the ventral visual stream and motion areas of the dorsal visual stream in processing of auditory motion at the same point in time after motion onset. This argues against the view that visual motion areas, such as area V5, are preferentially recruited for auditory motion analysis in the blind. Rather, cross‐modal reorganization of cortical areas induced by blindness seems to be largely independent of the specific visual functions of the same areas in sighted persons.     

Orienting visuospatial attention generates manual reaction time asymmetries in target detection and pointing

Right-handers exhibit a left hand advantage in response preparation when pointing to targets. These manual asymmetries are generally attributed to a right hemisphere specialization for spatial processing. More precisely, the left hand reaction time (RT) advantage was recently supposed to reflect specifically the right hemisphere superiority for movement planning. This study proposes to investigate a possible attentional origin for manual RT asymmetries. In a first experiment, we used the covert orienting of attention paradigm to measure subjects' RTs when reaching at targets (pointing task) both in valid, neutral and invalid conditions, either in the left or in the right visual fields and with the left and the right hand. In a second experiment, we applied the same paradigm to a detection task (key-pressing). Results revealed that orienting of attention to spatial locations was more time consuming when responding with the right than with the left hand, whether movement planning was required or not. It is suggested that the right hemisphere dominance for orienting of visuospatial attention account, partly at least, for the RT asymmetries classically observed in manual aiming.     

Covert and overt orienting to gaze direction cues and the effects of fixation offset

We examined covert and overt orienting in response to non-predictive gaze direction cues and investigated whether the subcortical superior colliculus (SC) plays a role in this type of orienting. Participants viewed a centrally presented gazing schematic face and responded to targets appearing at gazed-at or non-gazed-at locations either by making a keypress response while maintaining central fixation or by making an eye movement to the target. For both response conditions, the fixation stimulus (the gazing face) either remained on the screen or was extinguished at the time of target presentation, a manipulation known to engage and disengage the SC. Results revealed that participants making manual responses oriented covertly to the gazed-at location regardless of the fixation condition, and that participants making eye movements oriented overtly only if the fixation stimulus remained on the screen. Overt gaze-triggered orienting was not enhanced relative to covert orienting, and the fixation offset effect was not reduced for averted gaze cues relative to straight gaze cues. These findings suggest that gaze direction cues do not activate or predisengage the oculomotor system, and thus that orienting to gaze direction does not engage the SC. This is consistent with the view that gaze-triggered orienting is a unique form of reflexive orienting that depends crucially on cortical processes.