Neuronal responses in area 7a to multiple stimulus displays: II. responses are suppressed at the cued location.

Everyday visual scenes contain a variety of stimuli that vary in their significance. The companion paper demonstrates that neurons in the posterior parietal cortex (PPC) are capable of encoding the spatial locations of the salient stimulus in multiple stimulus scenes. The present experiment sought to address how neuronal responses to stimuli appearing in the receptive field are modulated after attention has been drawn to one of multiple stimuli in a visual scene. We recorded from area 7a of the PPC in monkeys trained to do a spatial version of a match-to-sample task. The results show that neuronal responses are greatly suppressed when stimuli appear at previously attended locations. No reduction in responsiveness is observed for locations where stimuli had previously appeared but did not draw attention. These results support the hypothesis that area 7a has a role in redirecting attention to stimuli appearing at novel, unattended locations.     

Neural correlates of spatial judgement during object construction in parietal cortex

We recorded the activity of parietal area 7a neurons in monkeys performing an object construction task. In each trial, a model object consisting of a variable arrangement of squares was presented, followed after a delay by a copy of the model object that was missing a single square. Monkeys replaced the missing square to reconstruct the model configuration. Activity of many 7a neurons varied systematically with the position of the missing square and predicted where monkeys were going to add parts to the object they were building. The location of the missing square was a computed spatial datum important to object construction which did not correlate with the retinal location of a visual stimulus or the direction of the required motor response. The population of cells coding this coordinate was generally inactive when the same spatial locations were made relevant by visual targets to which monkeys either planned saccades or directed attention in other behavioral contexts. The data suggest that some parietal neurons participate in neural representations of space that reflect spatial cognitive as opposed to sensorimotor processing, coding the results of spatial computations performed on visual stimuli to meet cognitive objectives.     

Persistent discharges in the prefrontal cortex of monkeys naive to working memory tasks

Neurons in the prefrontal cortex and a network of interconnected brain areas discharge in a persistent fashion after the offset of sensory stimulation. Such persistent discharges are thought to constitute a neuronal correlate of working memory. The information content of neuronal discharges and its anatomical localization across the surface of the prefrontal cortex has been a matter of debate. Discrepant results by different laboratories may be due to the effects of different training regiments and tasks used in memory tasks. In order to address how training in a memory task alters neuronal responses, we performed recordings in monkeys that were never trained in memory tasks, but passively viewed visual stimuli. We have found that a population of prefrontal neurons responded to visual stimuli and also exhibited significantly elevated responses during "delay" intervals of the task. For a population of these neurons, persistent discharges were selective for the location and feature of the preceding stimulus. These discharges were typically disrupted by the appearance of a subsequent stimulus. Our results suggest that some prefrontal neurons represent the location and identity of visual stimuli in a persistent fashion, even when the latter are not behaviorally important or required to be kept in memory.     

Human ventral parietal cortex plays a functional role on visuospatial attention and primary consciousness. A repetitive transcranial magnetic stimulation study

In this paper, we used repetitive transcranial magnetic stimulation (rTMS) in 18 normal subjects to investigate whether the ventral posterior parietal cortex (PPC) plays a causal role on visuospatial attention and primary consciousness and whether these 2 functions are linearly correlated with each other. Two distinct experimental conditions involved a similar visual stimuli recognition paradigm. In "Consciousness" experiment, number of consciously perceived visual stimuli was lower by about 10% after rTMS (300 ms, 20 Hz, motor threshold intensity) on left or right PPC than after sham (pseudo) rTMS. In "Attentional" Posner's experiment, these stimuli were always consciously perceived. Compared with sham condition, parietal rTMS slowed of about 25 ms reaction time to go stimuli, thus disclosing effects on endogenous covert spatial attention. No linear correlation was observed between the rTMS-induced impairment on attention and conscious perception. Results suggest that PPC plays a slight but significant causal role in both visuospatial attention and primary consciousness. Furthermore, these high-level cognitive functions, as modulated by parietal rTMS, do not seem to share either linear or simple relationships.     

Additive effects of emotional content and spatial selective attention on electrocortical facilitation

Affectively arousing visual stimuli have been suggested to automatically attract attentional resources in order to optimize sensory processing. The present study crosses the factors of spatial selective attention and affective content, and examines the relationship between instructed (spatial) and automatic attention to affective stimuli. In addition to response times and error rate, electroencephalographic data from 129 electrodes were recorded during a covert spatial attention task. This task required silent counting of random-dot targets embedded in a 10 Hz flicker of colored pictures presented to both hemifields. Steady-state visual evoked potentials (ssVEPs) were obtained to determine amplitude and phase of electrocortical responses to pictures. An increase of ssVEP amplitude was observed as an additive function of spatial attention and emotional content. Statistical parametric mapping of this effect indicated occipito-temporal and parietal cortex activation contralateral to the attended visual hemifield in ssVEP amplitude modulation. This difference was most pronounced during selection of the left visual hemifield, at right temporal electrodes. In line with this finding, phase information revealed accelerated processing of aversive arousing, compared to affectively neutral pictures. The data suggest that affective stimulus properties modulate the spatiotemporal process along the ventral stream, encompassing amplitude amplification and timing changes of posterior and temporal cortex.     

Neural activity in primate parietal area 7a related to spatial analysis of visual mazes

Cognitive psychological studies of humans and monkeys solving visual mazes have provided evidence that a covert analysis of the maze takes place during periods of eye fixation interspersed between saccades, or when mazes are solved without eye movements. We investigated the neural basis of this process in posterior parietal cortex by recording the activity of single neurons in area 7a during maze solution. Monkeys were required to determine from a single point of fixation whether a critical path through the maze reached an exit or a blind ending. We found that during this process the activity of approximately one in four neurons in area 7a was spatially tuned to maze path direction. We obtained evidence that path tuning did not reflect a covert saccade plan insofar as the majority of neurons active during maze solution were not active on a delayed-saccade control task, and the minority that were active on both tasks did not exhibit congruent spatial tuning in the two conditions. We also obtained evidence that path tuning during maze solution was not due to the locations of visual receptive fields mapped outside the behavioral context of maze solution, in that receptive field centers and preferred path directions were not spatially aligned. Finally, neurons tuned to path direction were not present in area 7a when a na?ve animal viewed the same visual maze stimuli but did not solve them. These data support the hypothesis that path tuning in parietal cortex is not due to the lower level visual features of the maze stimulus, but rather is associated with maze solution, and as such, reflects a cognitive process applied to a complex visual stimulus.     

Cortical substrates supporting visual search in humans.

Serial and parallel visual search tasks were presented to patients with focal lesions in dorsolateral frontal, lateral parietal, or temporal-parietal cortex. In the unilateral display conditions, search efficiency in all patient groups was similar to the normal control group for stimuli both on the ipsi- and on the contralesional side of the displays. In contrast, in the bilateral display conditions, all patient groups showed a marked delay in initiating search on the side contralateral to the lesion as compared to normal controls. This delay was more pronounced when attention demands on the ipsilateral side increased, either by making target-distractor discrimination more difficult (serial search task), or by increasing the number of ipsilateral distractor items. The contralateral deficit was evident in all patient groups, supporting the notion that dorsolateral frontal as well as posterior parietal and temporal-parietal cortex plays a critical role in visual spatial attention.     

Neuronal responses to optic flow in the monkey parietal area PEc

Area PEc, a high order association area, is located in the dorsocaudal portion of the superior parietal cortex. PEc neurons encode visual motion signals, especially the direction of stimulus motion. The present study tested if PEc neurons also process visual correlates of self-motion. The extracellular activity of single neurons in response to optic flow stimuli was recorded in two monkeys (Macaca fascicularis) trained in a fixation task. The stimuli were produced by random dots simulating planar motion, radial expansion and radial contraction. A substantial number of PEc neurons were specifically activated by radial optic flow and were selective for the position of the focus of expansion with respect to the fovea. Eccentric positions of the focus of expansion were preferred. Almost all neurons showed opponent excitatory-inhibitory activity to expanding-contracting visual fields. Planar motion elicited very weak responses. Optic flow responsiveness is not entirely explained by classical bar sensitivity in PEc neurons, suggesting that optic flow and classical bar responses could serve different mechanisms in the integration of visuo-motor signals to prepare body movements.     

Remapping attentional priorities: differential contribution of superior parietal lobule and intraparietal sulcus

Seeking and selectively attending to significant extrapersonal stimuli in a dynamic environment requires the updating of an attentional priority map. Using functional magnetic resonance imaging, we investigated the role of posterior parietal cortex in such remappings of attentional priorities where the configuration, location, and significance of stimuli were systematically varied. Our data revealed a functional dissociation between 2 juxtaposed posterior parietal regions: one in the superior parietal lobule (SPL) and another in the intraparietal sulcus (IPS). SPL was preferentially activated in all conditions where a spatial displacement occurred in the location of the target, the location of the distracter, or the focus of attention (exogenous and endogenous shifts of spatial attention). Shifts of the attentional focus also activated the IPS but principally if they were guided endogenously by internal rules of relevance rather than stimulus displacement per se (endogenous attention shifts). Only the IPS region was activated by transient resetting of target significance when the stimulus configuration changed but the attentional focus remained spatially fixed (feature attention shifts). These 2 components of the large-scale frontoparietal spatial attention network therefore have common and distinctive functions. In specific, the IPS component is more closely related to the compilation of an attentional priority map, including the endogenous recalibration of attentional weights. The SPL component, on the other hand, is more closely related to the modification of spatial coordinates linked to attentional priorities (spatial shifting). Collectively, these 2 areas allow posterior parietal cortex to dynamically encode extrapersonal events according to their spatial coordinates and valence.     

Perinatal-lesion-induced reorganization of cerebral functions revealed using reversible cooling deactivation and attentional tasks

We tested the concept that lesions of primary visual cortical areas 17 and 18 sustained on the day of birth induce a redistribution of cerebral operations underlying the ability to disengage visual attention and then redirect it to a new location. In cats, these operations are normally highly localizable to posterior middle suprasylvian (pMS) cortex. Three stimulation paradigms were used: (i) movement of a high contrast visual stimulus into the visual field; (ii) illumination of a static light-emitting diode (LED) stimulus; and (iii) a control static auditory stimulus. To test for the redistribution of critical neural operations, cryoloops were implanted bilaterally in the pMS sulcus and in contact with ventral posterior suprasylvian (vPS) cortex. Separate and combined deactivations of pMS and vPS cortices in cats with early lesions of primary visual cortex showed that full, unilateral deactivation of pMS cortex only partially impaired the ability to detect and orient to stimuli moved into the contracooled hemifield. Much more complete impairment required the additional deactivation of ipsilateral vPS cortex. Bilateral pMS deactivation alone, or in combination with bilateral vPS deactivation, largely reversed the unilateral contracooled neglect. For the orienting to static, illuminated LED stimuli, unilateral deactivation of pMS cortex was sufficient to fully impair orienting to stimuli presented in the contracooled hemifield. Bilateral pMS deactivation induced an almost complete visual-field-wide neglect of stimuli. On its own, unilateral deactivation of vPS cortex was without effect on either task, although bilateral vPS deactivations introduced inconsistencies into the performance. Termination of cooling reversed all deficits. Finally, neither the initial lesion of areas 17 and 18 nor cooling of either the MS or vPS cortex alone, or in combination, interfered with orienting to sound stimuli. Overall, our results provide evidence that at least one highly localizable visual function of normal cerebral cortex is remapped across the cortical surface following the early lesion of primary visual cortical areas 17 and 18. Moreover, the redistribution has spread the essential neural operations from the visual parietal cortex to a normally functionally distinct type of cortex in the visual temporal system.     

Spatially selective representations of voluntary and stimulus-driven attentional priority in human occipital, parietal, and frontal cortex

When multiple objects are present in a visual scene, they compete for cortical processing in the visual system; selective attention biases this competition so that representations of behaviorally relevant objects enter awareness and irrelevant objects do not. Deployments of selective attention can be voluntary (e.g., shift or attention to a target's expected spatial location) or stimulus driven (e.g., capture of attention by a target-defining feature such as color). Here we use functional magnetic resonance imaging to show that both of these factors induce spatially selective attentional modulations within regions of human occipital, parietal, and frontal cortex. In addition, the voluntary attentional modulations are temporally sustained, indicating that activity in these regions dynamically tracks the locus of attention. These data show that a convolution of factors, including prior knowledge of location and target-defining features, determines the relative competitive advantage of visual stimuli within multiple stages of the visual system.     

Dorsal posterior parietal rTMS affects voluntary orienting of visuospatial attention

Patients with lesions in posterior parietal cortex (PPC) are relatively unimpaired in voluntarily directing visual attention to different spatial locations, while many neuroimaging studies in healthy subjects suggest dorsal PPC involvement in this function. We used an offline repetitive transcranial magnetic stimulation (rTMS) protocol to study this issue further. Ten healthy participants performed a cue-target paradigm. Cues prompted covert orienting of spatial attention under voluntary control to either a left or right visual field position. Targets were flashed subsequently at the cued or uncued location, or bilaterally. Following rTMS over right dorsal PPC, (i) the benefit for target detection at cued versus uncued positions was preserved irrespective of cueing direction (left- or rightward), but (ii) leftward cueing was associated with a global impairment in target detection, at all target locations. This reveals that leftward orienting was still possible after right dorsal PPC stimulation, albeit at an increased overall cost for target detection. In addition, rTMS (iii) impaired left, but (iv) enhanced right target detection after rightward cueing. The finding of a global drop in target detection during leftward orienting with a spared, relative detection benefit at the cued (left) location (i-ii) suggests that right dorsal PPC plays a subsidiary rather than pivotal role in voluntary spatial orienting. This finding reconciles seemingly conflicting results from patients and neuroimaging studies. The finding of attentional inhibition and enhancement occurring contra- and ipsilaterally to the stimulation site (iii-iv) supports the view that spatial attention bias can be selectively modulated through rTMS, which has proven useful to transiently reduce visual hemispatial neglect.     

The interaction of brain regions during visual search processing as revealed by transcranial magnetic stimulation

Although it has long been known that right posterior parietal cortex (PPC) has a role in certain visual search tasks, and human motion area V5 is involved in processing tasks requiring attention to motion, little is known about how these areas may interact during the processing of a task requiring the speciality of each. Using transcranial magnetic stimulation (TMS), this study first established the specialization of each area in the form of a double dissociation; TMS to right PPC disrupted processing of a color/form conjunction and TMS to V5 disrupted processing of a motion/form conjunction. The key finding of this study is, however, if TMS is used to disrupt processing of V5 at its critical time of activation during the motion/form conjunction task, concurrent disruption of right PPC now has a significant effect, where TMS at PPC alone does not. Our findings challenge the conventional interpretation of the role of right PPC in conjunction search and spatial attention.     

The priming method: imaging unconscious repetition priming reveals an abstract representation of number in the parietal lobes.

Most of the current brain imaging methods are limited by the low spatial resolution of neuroimaging techniques and remain unable to measure activity at the scale of single neurons or small columns of neurons, which are the coding elements of the nervous system. In this work we have adapted the priming method, an emerging research strategy that can overcome some of these spatial limitations, to investigate the coding of numerical quantities in the human brain. This approach combines the logic of psychological priming experiments with the recently discovered neurophysiological phenomenon called repetition suppression (RS). In each trial, while subjects perform a constant task, a subliminal prime is presented prior to each target. By varying the relationship between prime and target, one can detect which brain areas present RS specifically for any given level of prime-target repetition. We first expose the general logic, potential and limitations of the priming method and then illustrate it by demonstrating that a region of parietal cortex is coding for numbers at the quantity level, independently of other stimulus attributes, and that this region processes both consciously and unconsciously perceived stimuli.     

A pure salience response in posterior parietal cortex

When exploring a visual scene, some objects perceptually popout because of a difference of color, shape, or size. This bottom-up information is an important part of many models describing the allocation of visual attention. It has been hypothesized that the lateral intraparietal area (LIP) acts as a "priority map," integrating bottom-up and top-down information to guide the allocation of attention. Despite a large literature describing top-down influences in LIP, the presence of a pure salience response to a salient stimulus defined by its static features alone has not been reported. We compared LIP responses with colored salient stimuli and distractors in a passive fixation task. Many LIP neurons responded preferentially to 1 of the 2 colored stimuli, yet the mean responses to the salient stimuli were significantly higher than to distractors, independent of the features of the stimuli. These enhanced responses were significant within 75 ms, and the mean responses to salient and distractor stimuli were tightly correlated, suggesting a simple gain control. We propose that a pure salience signal rapidly appears in LIP by collating salience signals from earlier visual areas. This contributes to the creation of a priority map, which is used to guide attention and saccades.     

Role of parietal cortex and hippocampus in representing spatial information.

Rats with lesions in the parietal cortex or hippocampus as well as cortical lesion and sham-operated controls were tested for acquisition or retention of a cheese board spatial task (dry land version of a water maze task). Results indicated that, relative to controls, rats with hippocampal or parietal cortex lesions were impaired in both acquisition and retention of the spatial task as measured by increased distances traveled to find the correct food location. It is suggested that both the hippocampus and parietal cortex subserve spatial representations required for optimal learning and performance of the cheese board spatial task.     

Three-dimensional structure-from-motion selectivity in the anterior superior temporal polysensory area, STPa, of the behaving monkey

Human and non-human primates are able to perceive three-dimensional structure from motion displays. Three-dimensional structure-from-motion (object-motion) displays were used to test the hypothesis that neurons in the anterior division of the superior temporal polysensory area (STPa) of monkeys can selectively respond to three-dimensional structure-from-motion. Monkeys performed a reaction time task that required the detection of a change in the fraction of structure in three-dimensional transparent sphere displays. Neurons were able to distinguish structured and unstructured three-dimensional optic flow. These cells could differentiate the change in structure-from-motion at stimulus presentation and when the animal was detecting the amount of structure in the display. Some of these neurons were also tuned for characteristics of the sphere stimuli. Cells were also tested with navigational motion and many were found to respond both to three-dimensional structure-from-motion and navigational motion. These results suggest that STPa neurons represent specific aspects of three-dimensional surface structure and that neurons within STPa contribute to the perception of three-dimensional structure-from-motion.     

Cortical mechanisms for shifting and holding visuospatial attention

Access to visual awareness is often determined by covert, voluntary deployments of visual attention. Voluntary orienting without eye movements requires decoupling attention from the locus of fixation, a shift to the desired location, and maintenance of attention at that location. We used event-related functional magnetic resonance imaging to dissociate these components while observers shifted attention among 3 streams of letters and digits, one located at fixation and 2 in the periphery. Compared with holding attention at the current location, shifting attention between the peripheral locations was associated with transient increases in neural activity in the superior parietal lobule (SPL) and frontal eye fields (FEF), as in previous studies. The supplementary eye fields and separate portions of SPL and FEF were more active for decoupling attention from fixation than for shifting attention to a new location. Large segments of precentral sulcus (PreCS) and posterior parietal cortex (PPC) were more active when attention was maintained in the periphery than when it was maintained at fixation. We conclude that distinct subcomponents of the dorsal frontoparietal network initiate redeployments of covert attention to new locations and disengage attention from fixation, while sustained activity in lateral regions of PPC and PreCS represents sustained states of peripheral attention.     

Dissociation of stimulus relevance and saliency factors during shifts of visuospatial attention

The control of visuospatial attention entails multiple processes, including both voluntary (endogenous) factors and stimulus-driven (exogenous) factors. Exogenous processes can be triggered by visual targets presented at a previously unattended location, thus capturing attention in a stimulus-driven manner. However, little is known about the relative role of stimulus salience and behavioral relevance for this type of spatial reorienting. Here, we directly assessed how salience and relevance affect activation of the frontoparietal attentional system, using either low-salience but task-relevant target stimuli or salient but task-irrelevant flickering checkerboards. We compared event-related functional magnetic resonance imaging responses for stimuli presented at the unattended versus attended side (invalid minus valid trials), separately for the 2 categories of visual stimuli. We found that task-relevant invalid targets activated the frontoparietal attentional network, demonstrating that this system engages when target stimuli are presented at an unattended location, even when these have a low perceptual salience. Conversely, the presentation of high-salience checkerboards in one hemifield while endogenous attention was engaged elsewhere did not activate the attentional network. These findings indicate that task relevance is critical for stimulus-driven engagement of the attentional network when attentional resources are endogenously allocated somewhere else.     

Parieto-frontal interactions in visual-object and visual-spatial working memory: evidence from transcranial magnetic stimulation.

This study aimed to investigate whether transcranial magnetic stimulation (TMS) can induce selective working memory (WM) deficits of visual-object versus visual-spatial information in normal humans. Thirty-five healthy subjects performed two computerized visual n-back tasks, in which they were required to memorize spatial locations or abstract patterns. In a first series of experiments, unilateral or bilateral TMS was delivered on posterior parietal and middle temporal regions of both hemispheres after various delays during the WM task. Bilateral temporal TMS increased reaction times (RTs) in the visual-object, whereas bilateral parietal TMS selectively increased RTs in the visual-spatial WM task. These effects were evident at a delay of 300 ms. Response accuracy was not affected by bilateral or unilateral TMS of either cortical region. In a second group of experiments, bilateral TMS was applied over the superior frontal gyrus (SFG) or the dorsolateral prefrontal cortex (DLPFC). TMS of the SFG selectively increased RTs in the visual-spatial WM task, whereas TMS of the DLPFC interfered with both WM tasks, in terms of both accuracy and RTs. These effects were evident when TMS was applied after a delay of 600 ms, but not one of 300 ms. These findings confirm the segregation of WM buffers for object and spatial information in the posterior cortical regions. In the frontal cortex, the DLPFC appears to be necessary for WM computations regardless of the stimulus material.