Topographic maps of visual spatial attention in human parietal cortex

Functional magnetic resonance imaging (fMRI) was used to measure activity in human parietal cortex during performance of a visual detection task in which the focus of attention systematically traversed the visual field. Critically, the stimuli were identical on all trials (except for slight contrast changes in a fully randomized selection of the target locations) whereas only the cued location varied. Traveling waves of activity were observed in posterior parietal cortex consistent with shifts in covert attention in the absence of eye movements. The temporal phase of the fMRI signal in each voxel indicated the corresponding visual field location. Visualization of the distribution of temporal phases on a flattened representation of parietal cortex revealed at least two distinct topographically organized cortical areas within the intraparietal sulcus (IPS), each representing the contralateral visual field. Two cortical areas were proposed based on this topographic organization, which we refer to as IPS1 and IPS2 to indicate their locations within the IPS. This nomenclature is neutral with respect to possible homologies with well-established cortical areas in the monkey brain. The two proposed cortical areas exhibited relatively little response to passive visual stimulation in comparison with early visual areas. These results provide evidence for multiple topographic maps in human parietal cortex.     

Enhanced visual spatial attention ipsilateral to rTMS-induced 'virtual lesions' of human parietal cortex

The breakdown of attentional mechanisms after brain damage can have drastic behavioral consequences, as in patients suffering from spatial neglect. While much research has concentrated on impaired attention to targets contralateral to sites of brain damage, here we report the ipsilateral enhancement of visual attention after repetitive transcranial magnetic stimulation (rTMS) of parietal cortex at parameters known to reduce cortical excitability. Normal healthy subjects received rTMS (1 Hz, 10 mins) over right or left parietal cortex. Subsequently, detection of visual stimuli contralateral to the stimulated hemisphere was consistently impaired when stimuli were also present in the opposite hemifield, mirroring the extinction phenomenon commonly observed in neglect patients. Additionally, subjects' attention to ipsilateral targets improved significantly over normal levels. These results underline the potential of focal brain dysfunction to produce behavioral improvement and give experimental support to models of interhemispheric competition in the distributed brain network for spatial attention.     

Influences of lesions of parietal cortex on visual spatial attention in humans

Summary Several brain areas have been identified with attention, because damage to these regions leads to neglect and extinction. We have tested elements of visual attentional processing in patients with parietal, frontal, or temporal lesions and compared their responses to control subjects. Normal humans respond faster in a reaction time task when the spatial location of a target is correctly predicted by an antecedent stimulus (valid cue) than when the location is incorrectly predicted (invalid cue). The cue is hypothesized to shift attention towards its location and thereby facilitate or impede response latencies. The reaction times of individuals with damage to the parietal lobe are somewhat slowed for targets ipsilateral or contralateral to the side of the lesion if the targets are preceded by valid cues. These same patients are extremely slow in responding to targets in the visual field contralateral to the lesion when the cue has just appeared in the unaffected (ipsilateral) visual field. In addition, these individuals are especially slow in responding to targets in either visual field when the lights are preceded by weak, diffuse illumination of the entire visual field. Patients with lesions of the frontal lobe have very slow reaction times in general and, as is the case for patients with lesions of the temporal lobe, are slow in all conditions for targets in the field contralateral to the lesion. These patterns are probably not associated with attentional defects. For patients with parietal lesions, these studies demonstrate a further deficit in a cued reaction-time task suggesting abnormal visual attention. Since different sites of brain damage yield different patterns of responses, tests such as these could be of analytic and diagnostic value.     

Inactivation of parietal and prefrontal cortex reveals interdependence of neural activity during memory-guided saccades

Dorsolateral prefrontal and posterior parietal cortex share reciprocal projections. They also share nearly identical patterns of neuronal activation during performance of memory-guided saccades. To test the hypothesis that the reciprocal projections between parietal and prefrontal neurons may entrain their parallel activation, the present experiments have combined cortical cooling in one cortical area with single-unit recording in the other to more precisely determine the physiological interactions between the two during working memory performance. The activity of 105 cortical neurons during the performance of an oculomotor delayed response (ODR) task (43 parietal neurons during prefrontal cooling, 62 prefrontal neurons during parietal cooling) was compared across two blocks of trials collected while the distant cortical area either was maintained at normal body temperature or cooled. The mean firing rates of 71% of the prefrontal neurons during ODR performance changed significantly when parietal cortex was cooled. Prefrontal neurons the activity of which was modulated during the cue, delay, or saccade periods of the task were equally vulnerable to parietal inactivation. Further, both lower and higher firing rates relative to the precool period were seen with comparable frequency. Similar results were obtained from the converse experiment, in which the mean firing rates of 76% of the parietal neurons were significantly different while prefrontal cortex was cooled, specifically in those task epochs when the activity of each neuron was modulated during ODR performance. These effects again were seen equally in all epochs of the ODR task in the form of augmented or suppressed activity. Significant effects on the latency of neuronal activation during cue and saccade periods of the task were absent irrespective of the area cooled. Cooling was associated in some cases with a shift in the best direction of Gaussian tuning functions fit to neuronal activity, and these shifts were on average larger during parietal than prefrontal cooling. In view of the parallel between the similarity in activity patterns previously reported and the largely symmetrical cooling effects presently obtained, the data suggest that prefrontal and parietal neurons achieve matched activation during ODR performance through a symmetrical exchange of neuronal signals between them; in both cortical areas, neurons activated during the cue, delay, and also saccade epochs of the ODR task participate in reciprocal neurotransmission; and the output of each cortical area produces a mixture of excitatory and inhibitory drives within its target.     

Disentangling gaze shifts from preparatory ERP effects during spatial attention

After a cue directing attention to one side, anterior event-related potentials (ERPs) show contralateral negativity (anterior directing attention negativity, ADAN). It is unclear whether ADAN effects are contaminated by contralateral negativity arising from residual gaze shifts. Conversely, it is possible that ADAN-related potentials contaminate the horizontal electrooculogram (HEOG), via volume conduction. To evaluate these possibilities, we used high-resolution infrared eye tracking while recording EEG and HEOG in a cued spatial-attention task. We found that, after conventional ERP and HEOG preprocessing exclusions, small but systematic residual gaze shifts in the cued direction can remain, as revealed by the infrared measure. Nevertheless, by using this measure for more stringent exclusion of small gaze shifts, we confirmed that reliable ADAN components remain for preparatory spatial attention in the absence of any systematic gaze shifts toward the cued side.     

Neural correlates of sustained spatial attention in human early visual cortex

Attention is thought to enhance perceptual performance at attended locations through top-down attention signals that modulate activity in visual cortex. Here, we show that activity in early visual cortex is sustained during maintenance of attention in the absence of visual stimulation. We used functional magnetic resonance imaging (fMRI) to measure activity in visual cortex while human subjects performed a visual detection task in which a variable-duration delay period preceded target presentation. Portions of cortical areas V1, V2, and V3 representing the attended part of the visual field exhibited sustained increases in activity throughout the delay period. Portions of these cortical areas representing peripheral, unattended parts of the visual field displayed sustained decreases in activity. The data were well fit by a model that assumed the sustained neural activity was constant in amplitude over a time period equal to that of the actual delay period for each trial. These results demonstrate that sustained attention responses are present in early visual cortex (including primary visual cortex), in the absence of a visual stimulus, and that these responses correlate with the allocation of visuospatial attention in both the spatial and temporal domains.     

Fast and slow parietal pathways mediate spatial attention

Mechanisms of selective attention are vital for guiding human behavior. The parietal cortex has long been recognized as a neural substrate of spatial attention, but the unique role of distinct parietal subregions has remained unclear. Using single-pulse transcranial magnetic stimulation, we found that the angular gyrus of the right parietal cortex mediates spatial orienting during two distinct time periods after the onset of a behaviorally relevant event. The biphasic involvement of the angular gyrus suggests that both fast and slow visual pathways are necessary for orienting spatial attention.     

Perceiving numbers causes spatial shifts of attention

Number symbols are part of our everyday visual world. Here we show that merely looking at numbers causes a shift in covert attention to the left or right side, depending upon the number's magnitude. This observation implies obligatory activation of number meaning and signals a tight coupling of internal and external representations of space.     

The time course of cortical facilitation during cued shifts of spatial attention

Adaptive behavior requires the rapid switching of attention among potentially relevant stimuli that appear in the environment. The present study used an electrophysiological approach to continuously measure the time course of visual pathway facilitation in human subjects as attention was shifted from one location to another. Steady-state visual evoked potentials (SSVEPs) were recorded to rapidly flickering lights at attended and unattended locations, and variations in SSVEP amplitude over time were calculated after a cue to shift attention. The build-up of cortical facilitation reflected in SSVEP amplitude was found to bear a close temporal relationship with the emergence of accurate target discriminations at the newly attended location.     

Temporal structure in neuronal activity during working memory in macaque parietal cortex

Many cortical structures have elevated firing rates during working memory, but it is not known how the activity is maintained. To investigate whether reverberating activity is important, we studied the temporal structure of local field potential (LFP) activity and spiking from area LIP in two awake macaques during a memory-saccade task. Using spectral analysis, we found spatially tuned elevated power in the gamma band (25-90 Hz) in LFP and spiking activity during the memory period. Spiking and LFP activity were also coherent in the gamma band but not at lower frequencies. Finally, we decoded LFP activity on a single-trial basis and found that LFP activity in parietal cortex discriminated between preferred and anti-preferred direction with approximately the same accuracy as the spike rate and predicted the time of a planned movement with better accuracy than the spike rate. This finding could accelerate the development of a cortical neural prosthesis.     

Facilitation of neuronal activity in somatosensory and posterior parietal cortex during prehension

In order to study prehension in a reproducible manner, we trained monkeys to perform a task in which rectangular, spherical, and cylindrical objects were grasped, lifted, held, and lowered in response to visual cues. The animal’s hand movements were monitored using digital video, together with simultaneously recorded spike trains of neurons in primary somatosensory cortex (S-I) and posterior parietal cortex (PPC). Statistically significant task-related modulation of activity occurred in 78% of neurons tested in the hand area; twice as many cells were facilitated during object acquisition as were depressed. Cortical neurons receiving inputs from tactile receptors in glabrous skin of the fingers and palm, hairy skin of the hand dorsum, or deep receptors in muscles and joints of the hand modulated their firing rates during prehension in consistent and reproducible patterns. Spike trains of individual neurons differed in duration and amplitude of firing, the particular hand behavior(s) monitored, and their sensitivity to the shape of the grasped object. Neurons were classified by statistical analysis into groups whose spike trains were tuned to single task stages, spanned two successive stages, or were multiaction. The classes were not uniformly distributed in specific cytoarchitectonic fields, nor among particular somatosensory modalities. Sequential deformation of parts of the hand as the task progressed was reflected in successive responses of different members of this population. The earliest activity occurred in PPC, where 28% of neurons increased firing prior to hand contact with objects; such neurons may participate in anticipatory motor control programs. Activity shifted rostrally to S-I as the hand contacted the object and manipulated it. The shape of the grasped object had the strongest influence on PPC cells. The results suggest that parietal neurons monitor hand actions during prehension, as well as the physical properties of the grasped object, by shifting activity between populations responsive to hand shaping, grasping, and manipulatory behaviors. Received: 1 October 1998 / Accepted: 4 May 1999     

Difficulty of perceptual spatiotemporal integration modulates the neural activity of left inferior parietal cortex

The integration of spatial and temporal information is a prerequisite for skilled movements. Likewise, spatial and temporal information must be integrated to predict the potential collision (or otherwise) of two moving objects. In a previous blocked functional magnetic resonance imaging (fMRI) study [Neuroimage 20 (2003) S82] we showed that collision judgments (relative to size judgments) provoked a significant increase in neural activity in the left inferior parietal cortex (supramarginal gyrus). This result suggests that this region is involved in the integration of perceptual spatiotemporal information in addition to its known involvement in programming skilled actions. To further investigate the impact of the integration of temporal and spatial information on the left parietal cortex we conducted an event-related fMRI study in which we varied the difficulty of the collision (and the size) judgment tasks parametrically. Reaction times and error rates were used as behavioral measures of increasing task demands. There was a significant linear increase in reaction times and error rates during the collision and the size tasks over the four levels of task difficulty. A linear increase of the blood oxygen level-dependent signal in the left inferior parietal cortex was found only for the collision, not for the size, conditions. Neural activation in the left inferior parietal cortex thus paralleled the increasing demands on spatiotemporal integration. This result confirms that the left supramarginal gyrus integrates spatial and temporal information irrespective of motor demands.     

Bilateral parietal cortex function during motor imagery

The aim of this study was to investigate the involvement of the parietal cortex during motor imagery (MI). In experiment one, participants imagined a sequence of upper limb movements during FMRI scanning. Statistical parametric mapping revealed a network of activation consistent with previous MI research, including activation in right and left inferior and superior parietal cortex. In experiment two, participants imagined a sequence of upper limb movements while real or sham single-pulse TMS was delivered over the scalp area corresponding to each individual’s left or right superior parietal cortex. At the end of each trial, participants moved their upper limbs to the position that would result from executing the sequence of movements. TMS degraded accuracy of MI compared to sham stimulation, and both accuracy and confidence decreased with real and sham stimulation later in the MI sequence. The effects of TMS were similar when delivered to either hemisphere. The results of this study provide evidence of the crucial role of SPL in MI, and may have implications for rehabilitation from brain injury.     

Auditory spatial discriminatory and mnemonic neurons in rat posterior parietal cortex

The present study was designed to investigate whether the rat posterior parietal cortex is involved in the perception and the representation of the auditory space. We recorded single neural activity in the posterior parietal cortex of rats that performed a directional delayed nonmatching-to-sample task. In the task, cue tones were presented in one of six speakers that were placed symmetrically around the rats. "Familiar tones" were those repeatedly used in the course of behavioral training. Novel tones were presented only during the unit recording time and less frequently used (e.g., only once in alternate weeks). The responses of the posterior parietal cortex neurons were typically tested with familiar cue tones while the rats were situated in a particular geomagnetic orientation. The same cells were further tested while the rats were reoriented by 180 degrees, or by novel cue tones. As the task included a delay period, in which the cue tone was removed, the rats had to maintain the directional information of the cue tones during this period to maximize the reward rates. A well-trained rat could perform the task with 85% success. We found two major types of neurons intermixed in the rat posterior parietal cortex. One type (n = 14) mainly discriminated the direction of the cue tones, whereas the other (n = 36) carried a mnemonic value of the cue tones while the tones were removed. The former responded only during the cue tone period (discriminatory neurons), whereas the latter responded during the cue tone period and the delay period (mnemonic neurons). These cells also exhibited broad directional tuning. The results agreed with previous studies, suggesting that a population coding scheme exists in the posterior parietal cortex. When the cells were tested with novel tones or when the rats were rotated through 180 degrees, the vast majority of the cells exhibited a directional tuning similar to those under the control conditions. Three quarters (18/24) of the cells that exhibited a mnemonic characteristic persisted in their directional preference when the rat's orientation was changed (12/17 neurons) or when an unfamiliar auditory stimulus was used (6/7 neurons). Half of the discriminatory neurons (4/8 neurons) persisted in their directional preference. These results, consistent with previous behavioral studies, suggest an allocentric representation of the auditory processing in this area. Furthermore, when the rat was reoriented or an unfamiliar cue tone was used, both the average and peak directional responses were enhanced in more than half of the mnemonic or discriminatory neurons. These results support the frequency-dependent neocortical gating hypothesis of the entorhinal hippocampal loop.     

Directional selectivity of BOLD activity in human posterior parietal cortex for memory-guided double-step saccades

We used functional magnetic resonance imaging (fMRI) to investigate the role of the human posterior parietal cortex (PPC) in storing target locations for delayed double-step saccades. To do so, we exploited the laterality of a subregion of PPC that preferentially responds to the memory of a target location presented in the contralateral visual field. Using an event-related design, we tracked fMRI signal changes in this region while subjects remembered the locations of two sequentially flashed targets, presented in either the same or different visual hemifields, and then saccaded to them in sequence. After presentation of the first target, the fMRI signal was always related to the side of the visual field in which it had been presented. When the second target was added, the cortical activity depended on the respective locations of both targets but was still significantly selective for the target of the first saccade. We conclude that this region within the human posterior parietal cortex not only acts as spatial storage center by retaining target locations for subsequent saccades but is also involved in selecting the target for the first intended saccade.     

Subcortical gating in the human visual system during spatial selective attention

The question of whether subcortical gating occurs as a function of spatial selective attention remains unsettled. This issue was investigated, using the paradigm of Eason et al. (1969) wherein subjects are instructed to attend to a specified location in a given visual field while attempting to ignore stimuli presented in the opposite field. Visual evoked responses falling within the 40-70 ms range were found to be significantly more negative when the location at which the evoking stimulus appeared was being attended to than when it was not. Also, later deflections (100-200 ms) were enhanced in amplitude and negatively biased. The very early effect provides further evidence for spatial attention-induced precortical gating. The later effects provide additional evidence for the amplitude enhancement of 'exogenous' components, along with the possible involvement of glial cell activity in the generation of slow wave negativity.     

Hemispheric asymmetry in memory-guided pointing during single-pulse transcranial magnetic stimulation of human parietal cortex

Dorsal posterior parietal cortex (PPC) has been implicated through single-unit recordings, neuroimaging data, and studies of brain-damaged humans in the spatial guidance of reaching and pointing movements. The present study examines the causal effect of single-pulse transcranial magnetic stimulation (TMS) over the left and right dorsal posterior parietal cortex during a memory-guided "reach-to-touch" movement task in six human subjects. Stimulation of the left parietal hemisphere significantly increased endpoint variability, independent of visual field, with no horizontal bias. In contrast, right parietal stimulation did not increase variability, but instead produced a significantly systematic leftward directional shift in pointing (contralateral to stimulation site) in both visual fields. Furthermore, the same lateralized pattern persisted with left-hand movement, suggesting that these aspects of parietal control of pointing movements are spatially fixed. To test whether the right parietal TMS shift occurs in visual or motor coordinates, we trained subjects to point correctly to optically reversed peripheral targets, viewed through a left-right Dove reversing prism. After prism adaptation, the horizontal pointing direction for a given visual target reversed, but the direction of shift during right parietal TMS did not reverse. Taken together, these data suggest that induction of a focal current reveals a hemispheric asymmetry in the early stages of the putative spatial processing in PPC. These results also suggest that a brief TMS pulse modifies the output of the right PPC in motor coordinates downstream from the adapted visuomotor reversal, rather than modifying the upstream visual coordinates of the memory representation.     

Specialization of reach function in human posterior parietal cortex

Posterior parietal cortex (PPC) plays an important role in the planning and control of goal-directed action. Single-unit studies in monkeys have identified reach-specific areas in the PPC, but the degree of effector and computational specificity for reach in the corresponding human regions is still under debate. Here, we review converging evidence spanning functional neuroimaging, parietal patient and transcranial magnetic stimulation studies in humans that suggests a functional topography for reach within human PPC. We contrast reach to saccade and grasp regions to distinguish functional specificity and also to understand how these different goal-directed actions might be coordinated at the cortical level. First, we present the current evidence for reach specificity in distinct modules in PPC, namely superior parietal occipital cortex, midposterior intraparietal cortex and angular gyrus, compared to saccade and grasp. Second, we review the evidence for hemispheric lateralization (both for hand and visual hemifield) in these reach representations. Third, we review evidence for computational reach specificity in these regions and finally propose a functional framework for these human PPC reach modules that includes (1) a distinction between the encoding of reach goals in posterior–medial PPC as opposed to reach movement vectors in more anterior–lateral PPC regions, and (2) their integration within a broader cortical framework for reach, grasp and eye–hand coordination. These findings represent both a confirmation and extension of findings that were previously reported for the monkey.     

Effects of selective visual attention in the parietal and temporal areas of the human cortex using evoked potential data

Studies of 11 young subjects addressed the analysis of evoked potentials in the parietal and temporal areas to sequential presentation of visual symbols on the left and right sides; symbols were squares and circles and were observed passively and in conditions of selective attention to target stimuli presented to the subjects in random order and requiring rapid and precise motor responses. Comparison of monopolar evoked potentials in leads P3, P4, T3, T4, T5, and T6 with bipolar potentials in leads P3-T3, P3-T5, P4-T4, and P4-T6 in conditions of passive and selective attention showed that voluntary attention was accompanied by significant rearrangements in evoked activity in the parietal and temporal areas. This was evident as: 1) an increase in correlations between evoked potentials in the parietal and temporal areas; 2) stabilization of monopolar evoked potentials over time, i.e., increases in the correlations of sequential evoked potentials, in both associative visual areas; 3) stabilization of bipolar parietal-temporal evoked potentials in terms of increases in their sequential correlations. It is suggested that selective attention facilitates linked activity of the two associative areas, which is needed for performance of visual selection.Translated from Rossiiskii Fiziologicheskii Zhurnal imeni I. M. Sechenova, Vol. 89, No. 7, pp. 776–785, July, 2003.