Lateral Intraparietal Research Articles

Dynamic Circuitry for Updating Spatial Representations. III. From Neurons to Behavior

Each time the eyes move, the visual system must adjust internal representations to account for the accompanying shift in the retinal image. In the lateral intraparietal cortex (LIP), neurons update the spatial representations of salient stimuli when the eyes move. In previous experiments, we found that split-brain monkeys were impaired on double-step saccade sequences that required updating across visual hemifields, as compared to within hemifield. Here we describe a subsequent experiment to characterize the relationship between behavioral performance and neural activity in LIP in the split-brain monkey. We recorded from single LIP neurons while split-brain and intact monkeys performed two conditions of the double-step saccade task: one required across-hemifield updating and the other required within-hemifield updating. We found that, despite extensive experience with the task, the split-brain monkeys were significantly more accurate for within-hemifield than for across-hemifield sequences. In parallel, we found that population activity in LIP of the split-brain monkeys was significantly stronger for the within-hemifield than for the across-hemifield condition of the double-step task. In contrast, in the normal monkey, both the average behavioral performance and population activity showed no bias toward the within-hemifield condition. Finally, we found that the difference between within-hemifield and across-hemifield performance in the split-brain monkeys was reflected at the level of single-neuron activity in LIP. These findings indicate that remapping activity in area LIP is present in the split-brain monkey for the double-step task and covaries with spatial behavior on within-hemifield compared to across-hemifield sequences.

Postsaccadic Activities in the Posterior Parietal Cortex of Primates Are Influenced by both Eye Movement Vectors and Eye Position

Primates explore their visual environment by redirecting the gaze to objects of interest by alternating eye movements and periods of steady fixation. During this task, the fixation point changes frequently in depth. Therefore, the representation of object location based on retinal disparity requires frequent updating. Neural activity was recorded in the lateral intraparietal (LIP) area while monkeys performed saccades between targets in different depths. We report that in the early postsaccadic period, posterior parietal neurons continue to encode the difference in depth between fixation point and targets. About one-third of these neurons are, during the same period, modulated by eye position in depth as well. In the late postsaccadic period, the influence of the previous movement vector dissipates, and parietal neurons are modulated only by the new fixation distance. This result suggests that the postsaccadic activity of area LIP contributes to the dynamic representation of the visual space, and it is compatible with the presence of both a vector subtraction computation and eye-position-dependent gain fields.

Parietal and superior frontal visuospatial maps activated by pointing and saccades

A recent study from our laboratory demonstrated that parietal cortex contains a map of visual space related to saccades and spatial attention and identified this area as the likely human homologue of the lateral intraparietal (LIP). A human homologue for the parietal reach region (PRR), thought to preferentially encode planned hand movements, has also been recently proposed. Both of these areas, originally identified in the macaque monkey, have been shown to encode space with eye-centered coordinates. Functional magnetic resonance imaging (fMRI) of humans was used to test the hypothesis that the putative human PRR contains a retinotopic map recruited by finger pointing but not saccades and to test more generally for differences in the visuospatial maps recruited by pointing and saccades. We identified multiple maps in both posterior parietal cortex and superior frontal cortex recruited for eye and hand movements, including maps not observed in previous mapping studies. Pointing and saccade maps were generally consistent within single subjects. We have developed new group analysis methods for phase-encoded data, which revealed subtle differences between pointing and saccades, including hemispheric asymmetries, but we did not find evidence of pointing-specific maps of visual space.

Separate Coding of Different Gaze Directions in the Superior Temporal Sulcus and Inferior Parietal Lobule

SummaryElectrophysiological recording in the anterior superior temporal sulcus (STS) of monkeys has demonstrated separate cell populations responsive to direct and averted gaze 1, 2. Human functional imaging has demonstrated posterior STS activation in gaze processing, particularly in coding the intentions conveyed by gaze 3, 4, 5, 6, but to date has provided no evidence of dissociable coding of different gaze directions. Because the spatial resolution typical of group-based fMRI studies (∼6–10 mm) exceeds the size of cellular patches sensitive to different facial characteristics (1–4 mm in monkeys), a more sensitive technique may be required. We therefore used fMRI adaptation, which is considered to offer superior resolution [7], to investigate whether the human anterior STS contains representations of different gaze directions, as suggested by non-human primate research. Subjects viewed probe faces gazing left, directly ahead, or right. Adapting to leftward gaze produced a reduction in BOLD response to left relative to right (and direct) gaze probes in the anterior STS and inferior parietal cortex; rightward gaze adaptation produced a corresponding reduction to right gaze probes. Consistent with these findings, averted gaze in the adapted direction was misidentified as direct. Our study provides the first human evidence of dissociable neural systems for left and right gaze.

A Magnitude Code Common to Numerosities and Number Symbols in Human Intraparietal Cortex

Activation of the horizontal segment of the intraparietal sulcus (hIPS) has been observed in various number-processing tasks, whether numbers were conveyed by symbolic numerals (digits, number words) or by nonsymbolic displays (dot patterns). This suggests an abstract coding of numerical magnitude. Here, we critically tested this hypothesis using fMRI adaptation to demonstrate notation-independent coding of numerical quantity in the hIPS. Once subjects were adapted either to dot patterns or to Arabic digits, activation in the hIPS and in frontal regions recovered in a distance-dependent fashion whenever a new number was presented, irrespective of notation changes. This remained unchanged when analyzing the hIPS peaks from an independent localizer scan of mental calculation. These results suggest an abstract coding of approximate number common to dots, digits, and number words. They support the idea that symbols acquire meaning by linking neural populations coding symbol shapes to those holding nonsymbolic representations of quantities.

Does tool-related fMRI activity within the intraparietal sulcus reflect the plan to grasp?

Neuroimaging investigations reliably describe a left-lateralized network of areas as underlying the representations of knowledge about familiar tools. Among the critical ‘nodes’ of the network, an area centered within the left intraparietal sulcus (IPS) is thought to be related to the motoric representations associated with familiar tools and their usage. This area is in the vicinity of an area implicated in the control of object-directed grasping actions: the anterior intraparietal area, AIP. The current study aimed to evaluate whether this tool-related intraparietal activity could be accounted for by the graspable nature of tools or whether it was due to additional factors such as the functionality of tools. First, we found that during a naming task activation within a discrete region of the left anterior intraparietal cortex was higher for tools than for graspable objects, but did not differ between graspable and non-graspable objects. In addition, the peak activity associated with tool naming was found to be largely distinct and consistently posterior to that associated with real object grasping. A separate region, anterior to the tool-selective focus and possibly overlapping with AIP, demonstrated weak selectivity for both tools and graspable objects relative to non-graspable objects.These findings indicate that this tool-selective area at the anterior end of the left IPS is both separable from the grasp-related intraparietal activity and, consistently, it does not simply reflect the processing of grasping affordances. Taken together, these results suggest that object graspability alone cannot account for the left intraparietal activity driven by the naming of tools. Instead, this activity may relate to learned motor representations associated with the skillful use of familiar tools.

Evidence for time‐variant decision making

Computational models based on diffusion processes have been proposed to account for human decision-making behaviour in a variety of tasks. The basic idea is that the brain keeps accumulating noisy sensory evidence until a critical level is reached. This study explores whether such models account for the speed and accuracy of perceptual decisions in a reaction-time random dot motion direction discrimination task, and whether they explain the decision-related activity of neurons recorded from the parietal cortex (area LIP) of monkeys performing the task. While a simple diffusion model can explain the psychometric function and the mean response times of correct responses, it fails to account for the longer response times observed for errors and for the response time distributions. Here I demonstrate that a time-variant version of the diffusion model can explain the psychometric function, the mean response times and the shape of the response time distributions. Such a time-variant mechanism could be implemented in different ways, but the best match between the physiological data and model predictions is provided by a diffusion process with a gain of the sensory signals, which increases over time. It can be shown that such a time-variant decision process allows the monkey to perform optimally (in the sense of maximizing reward rate) given the risk of aborting a trial by breaking fixation before a choice can be reported. The results suggest that the brain trades off speed and accuracy not only by adjusting parameters between trials but also by dynamic adjustments during an ongoing decision.

Temporal Processing of Saccade Targets in Parietal Cortex Area LIP During Visual Search

We studied whether the lateral intraparietal (LIP) area-a subdivision of parietal cortex anatomically interposed between visual cortical areas and saccade executive centers-contains neurons with activity patterns sufficient to contribute to the active process of selecting saccade targets in visual search. Visually responsive neurons were recorded while monkeys searched for a color-different target presented concurrently with seven distractors evenly distributed in a circular search array. We found that LIP neurons initially responded indiscriminately to the presentation of a visual stimulus in their response fields, regardless of its feature and identity. Their activation nevertheless evolved to signal the search target before saccade initiation: an ideal observer could reliably discriminate the target from the individual activation of 60% of neurons, on average, 138 ms after stimulus presentation and 26 ms before saccade initiation. Importantly, the timing of LIP neuronal discrimination varied proportionally with reaction times. These findings suggest that LIP activity reflects the selection of both the search target and the targeting saccade during active visual search.

Can One Suppress Subliminal Words?

Subliminal words cause behavioral priming, yet the depth of their processing remains debated. Using transcranial magnetic stimulation (TMS), Nakamura et al. demonstrate in this issue of Neuron that this subliminal priming effect can be selectively disrupted. Distinct TMS sites disrupt priming in lexical decision and pronunciation tasks, suggesting that task set influences subliminal processing.

Comparison of Shape Encoding in Primate Dorsal and Ventral Visual Pathways

Ventral and dorsal visual pathways perform fundamentally different functions. The former is involved in object recognition, whereas the latter carries out spatial localization of stimuli and visual guidance of motor actions. Despite the association of the dorsal pathway with spatial vision, recent studies have reported shape selectivity in the dorsal stream. We compared shape encoding in anterior inferotemporal cortex (AIT), a high-level ventral area, with that in lateral intraparietal cortex (LIP), a high-level dorsal area, during a fixation task. We found shape selectivities of individual neurons to be greater in anterior inferotemporal cortex than in lateral intraparietal cortex. At the neural population level, responses to different shapes were more dissimilar in AIT than LIP. Both observations suggest a greater capacity in AIT for making finer shape distinctions. Multivariate analyses of AIT data grouped together similar shapes based on neural population responses, whereas such grouping was indistinct in LIP. Thus in a first comparison of shape response properties in late stages of the two visual pathways, we report that AIT exhibits greater capability than LIP for both object discrimination and generalization. These differences in the two visual pathways provide the first neurophysiological evidence that shape encoding in the dorsal pathway is distinct from and not a mere duplication of that formed in the ventral pathway. In addition to shape selectivity, we observed stimulus-driven cognitive effects in both areas. Stimulus repetition suppression in LIP was similar to the well-known repetition suppression in AIT and may be associated with the "inhibition of return" memory effect observed during reflexive attention.

A Mirror Representation of Others' Actions in the Human Anterior Parietal Cortex

The anterior part of the human intraparietal sulcus is known to be involved in visually guided grasping. This region is also active during the observation of object manipulation by others. Here, we explore the nature of action representation using functional magnetic resonance imaging (fMRI). Fourteen subjects observed video clips showing object manipulation by the right or left hand. The clips were presented in either the right or left peripheral visual field. The fMRI activation in the occipital cortex and in the caudal sections of the parietal cortex was specific to the visual-field location of the clips. In contrast, the principal factor determining the response in anterior intraparietal cortex was the identity of the observed hand. Furthermore, these "hand-specific" parietal areas also showed contralateral hand specificity during self action (i.e., object manipulation) without visual feedback. A similar selectivity for the identity of the observed hand was seen when using a region of interest analysis, focusing on individually defined visuomotor voxels within the parietal cortex. This dual visuomotor grasping representation lends further evidence for the existence of a mirror system in humans and suggests that the anterior intraparietal cortex is involved in the specific motor simulation of hand actions.

Experience-dependent representation of visual categories in parietal cortex

Categorization is a process by which the brain assigns meaning to sensory stimuli. Through experience, we learn to group stimuli into categories, such as 'chair', 'table' and 'vehicle', which are critical for rapidly and appropriately selecting behavioural responses. Although much is known about the neural representation of simple visual stimulus features (for example, orientation, direction and colour), relatively little is known about how the brain learns and encodes the meaning of stimuli. We trained monkeys to classify 360 degrees of visual motion directions into two discrete categories, and compared neuronal activity in the lateral intraparietal (LIP) and middle temporal (MT) areas, two interconnected brain regions known to be involved in visual motion processing. Here we show that neurons in LIP--an area known to be centrally involved in visuo-spatial attention, motor planning and decision-making-robustly reflect the category of motion direction as a result of learning. The activity of LIP neurons encoded directions of motion according to their category membership, and that encoding shifted after the monkeys were retrained to group the same stimuli into two new categories. In contrast, neurons in area MT were strongly direction selective but carried little, if any, explicit category information. This indicates that LIP might be an important nexus for the transformation of visual direction selectivity to more abstract representations that encode the behavioural relevance, or meaning, of stimuli.

Neurons that know when to quit

With sufficient training, monkeys as well as people can be taught to ignore visually salient stimuli. Now Ipata and colleagues report that activity in monkey lateral intraparietal cortex (LIP) correlates with this ability to ignore salient stimuli, suggesting that activity in this area represents top-down modulation that adjusts visual salience.

Discrimination between active and passive head movements by macaque ventral and medial intraparietal cortex neurons

An important prerequisite for effective motor action is the discrimination between active and passive body movements. Passive movements often require immediate reflexes, whereas active movements may demand suppression of the latter. The vestibular system maintains correct body and head posture in space through reflexes. Since vestibular inputs have been reported to be largely suppressed in the vestibular nuclei during active head movements, we investigated whether head movement-related signals in the primate parietal cortex, a brain region involved in self-motion perception, could support both reflex functions and self-movement behaviour. We employed a paradigm that made available direct comparison of neuronal discharge under active and passive movement conditions. In this study, we demonstrate that a population of intraparietal (VIP (ventral) and MIP (medial)) cortex neurons change their preferred directions during horizontal head rotations depending on whether animals have performed active movements, or if they were moved passively. In other neurons no such change occurred. A combination of these signals would provide differential information about the active or passive nature of an ongoing movement. Moreover, some neurons' responses clearly anticipated the upcoming active head movement, providing a possible basis for vestibular-related reflex suppression. Intraparietal vestibular neurons thus distinguish between active and passive head movements, and their responses differ substantially from those reported in brainstem vestibular neurons, regarding strength, timing, and direction selectivity. We suggest that the contextual firing characteristics of these neurons have far-reaching implications for the suppression of reflex movements during active movement, and for the representation of space during self-movement.

Inter-individual Variability of the Facial Morphology During Conscious Smiling

Since many simulation and animation procedures for mimicry are based on averaged values and do not take into account an individual's situation, the goal of this study was to investigate the intra- and inter-individual variability of conscious smiling. Twenty-three surface points were marked on the faces of 31 adult test individuals. Six photographs of each subject's face were then taken under standardized conditions, one with a neutral facial expression and five while the individual was asked to smile (conscious smile "on command"). After digital superposition of the individual images (neutral and smiling) the displacements were measured for every measurement point on each individual. All data underwent statistical evaluation after normalization in the vertical and horizontal directions. Evaluation of intra- and inter-individual variability was carried out by analyzing the corresponding coefficients of variation and the formation of confidence intervals (confidence level 95%). The repeated measurements upon conscious smiling showed a moderate intra-individual variability with coefficients of variation under 10%. In contrast, the inter-individual variability of the measured values was relatively high. Here variation coefficients were measured of between 28% and 60% depending on the localization of the measuring point. The displacements' absolute magnitude was greatest in the lower facial third. The two corners of the mouth, the upper lip in the philtrum area, the cheeks and the side wings of the nose revealed the highest displacements. Due to the high inter-individual variability, an analysis based on averaged values or a simulation of the conscious smile must be viewed with a certain amount of criticism.

Brain Activity Related to Working Memory and Distraction in Children and Adults

In order to retain information in working memory (WM) during a delay, distracting stimuli must be ignored. This important ability improves during childhood, but the neural basis for this development is not known. We measured brain activity with functional magnetic resonance imaging in adults and 13-year-old children. Data were analyzed with an event-related design to isolate activity during cue, delay, distraction, and response selection. Adults were more accurate and less distractible than children. Activity in the middle frontal gyrus and intraparietal cortex was stronger in adults than in children during the delay, when information was maintained in WM. Distraction during the delay evoked activation in parietal and occipital cortices in both adults and children. However, distraction activated frontal cortex only in children. The larger frontal activation in response to distracters presented during the delay may explain why children are more susceptible to interfering stimuli.

Responses of neurons in the lateral intraparietal area to central visual cues

Goal-directed behavior is characterized by flexible stimulus-action mappings. The lateral intraparietal area (area LIP) contains a representation of extra-personal space that is used to guide goal-directed behavior. To examine further how area LIP contributes to these flexible stimulus-action mappings, we recorded LIP activity while rhesus monkeys participated in two different cueing tasks. In the first task, the color of a central light indicated the location of a monkey's saccadic endpoint in the absence of any other visual stimuli. In the second task, the color of a central light indicated which of two visual targets was the saccadic goal. In both tasks, LIP activity was modulated by these non-spatial cues. These observations further suggest a role for area LIP in mediating endogenous associations that link stimuli with actions.

Functional imaging of the intraparietal cortex during saccades to visual and memorized targets

The representation of perceived space and intended actions in the primate parietal cortex has been the subject of considerable debate. To address this issue, we used the quantitative 14C-deoxyglucose method to obtain maps of the activity pattern in the intraparietal cortex of rhesus monkeys executing saccades to visual and memorized targets. The principal effect induced by memory-guided saccades was found more caudally in the deepest part of the middle third of the lateral bank (within area LIPv) whereas that induced by visually guided saccades extended more rostrally and superficially in the anterior third of the bank (within area LIPd). The memory-saccade-related and the visual-saccade-related regions of activation overlapped only within area LIPv. Besides saccade execution, maximal activity in area LIPd required a visual stimulus. The region activated by visual fixation was located at the border of LIPv and LIPd, extending mainly within area LIPd, and occupying about one third of the neural space of the region activated for visual-saccades. We suggest that the lateral intraparietal cortex represents visual and motor space in segregated, albeit partially overlapping, regions.

Contribution of the Monkey Frontal Eye Field to Covert Visual Attention

The frontal eye field (FEF) has long been regarded as a cortical area critically involved in the execution of voluntary saccadic eye movements. However, recent studies have suggested that the FEF may also play a role in orienting attention. To address this issue, we reversibly inactivated the FEF using multiple microinjections of muscimol, a GABAA agonist, in two macaque monkeys performing visually guided saccades to a single target. The effects of FEF inactivation were also studied in a covert visual search task that required monkeys to search for a target presented among several distractors without making any eye movements. As expected, inactivating the FEF caused spatially selective deficits in executing visually guided saccades, but it also altered the ability to detect a visual target presented among distractors when no eye movements were permitted. These results allow us to conclude definitively to an involvement of the FEF in both oculomotor and attentional functions. Comparison of the present results with a similar experiment conducted in the lateral intraparietal cortex area revealed qualitatively different deficits, suggesting that the two areas may make distinct contributions to selective attention processes.

Activity in the Lateral Intraparietal Area Predicts the Goal and Latency of Saccades in a Free-Viewing Visual Search Task

The purpose of saccadic eye movements is to facilitate vision, by placing the fovea on interesting objects in the environment. Eye movements are not made for reward, and they are rarely restricted. Despite this, most of our knowledge about the neural genesis of eye movements comes from experiments in which specific eye movements are rewarded or restricted. Such experiments have demonstrated that activity in the lateral intraparietal (LIP) area of the monkey correlates with the monkey's planning of a memory-guided saccade or deciding where, on the basis of motion information, to make a saccade. However, other experiments have shown that neural activity in LIP can easily be dissociated from the generation of saccadic eye movements, especially when sophisticated behavioral paradigms dissociate the monkey's locus of attention from the goal of an intended saccade. In this study, we trained monkeys to report the results of a visual search task by making a nontargeting hand movement. Once the task began, the monkeys were entirely free to move their eyes, and rewards were not contingent on the monkeys making specific eye movements. We found that neural activity in LIP predicted not only the goal of the monkey's saccades but also their saccadic latencies.