Lateral Intraparietal Area Research Articles

Dynamic Integration of Task-Relevant Visual Features in Posterior Parietal Cortex

The primate visual system consists of multiple hierarchically organized cortical areas, each specialized for processing distinct aspects of the visual scene. For example, color and form are encoded in ventral pathway areas such as V4 and inferior temporal cortex, while motion is preferentially processed in dorsal pathway areas such as the middle temporal area. Such representations often need to be integrated perceptually to solve tasks that depend on multiple features. We tested the hypothesis that the lateral intraparietal area (LIP) integrates disparate task-relevant visual features by recording from LIP neurons in monkeys trained to identify target stimuli composed of conjunctions of color and motion features. We show that LIP neurons exhibit integrative representations of both color and motion features when they are task relevant and task-dependent shifts of both direction and color tuning. This suggests that LIP plays a role in flexibly integrating task-relevant sensory signals.

Encoding and decoding in parietal cortex during sensorimotor decision-making.

The lateral intraparietal area (LIP) of macaques has been asserted to play a fundamental role in sensorimotor decision-making. Here we dissect the neural code in LIP at the level of individual trial spike trains using a statistical approach based on generalized linear models. We show that LIP responses reflect a combination of temporally-overlapping task and decision-related signals. Our model accounts for the detailed statistics of LIP spike trains, and accurately predicts spike trains from task events on single trials. Moreover, we derive an optimal decoder for heterogeneous, multiplexed LIP responses that could be implemented in biologically plausible circuits. In contrast to interpretations of LIP as providing an instantaneous code for decision variables, we show that optimal decoding requires integrating LIP spikes over two timescales. These analyses provide a detailed understanding of the neural code in LIP, and a framework for studying the coding of multiplexed signals in higher brain areas.

Behavioral consequences of perceptual decision-making in oculomotor brain structures

Neurons in several oculomotor brain areas (such as the lateral intraparietal area and superior colliculus) carry a multitude of signals. Even within a single task, individual neurons may exhibit responses related to visual/sensory events, decision formation, and saccade execution. Little is known about whether these signals interact and if such interactions have functional consequences. To test for interactions between decision-making and saccade execution signals, we used a behavioral dual-task paradigm that measured saccade reaction time (SRT) to a decision-irrelevant target while observers conducted a motion direction discrimination task. Observers (n=5) judged the direction (leftward versus rightward) of a random dot motion stimulus (of variable coherence; speed: 5 °/s). At the offset of the dots, a target appeared either left or right side of the fixation point (displaced by 20°). Observers were instructed to make an eye movement to the target as quickly as possible. After the eye movement, the direction of preceding dot motion was reported with a button press. We tested whether the SRT to the target was affected by the direction and strength of motion stimuli presented during the direction-discrimination task. Indeed, SRTs were faster on congruent trials (when the direction of motion was same as the saccade direction) compared to incongruent trials (F1,4=26.23, p<0.01). Furthermore, SRTs progressively decreased with increased coherence (F4,16=5.45, p<0.05). Thus, simple visually-guided saccades were affected by the ongoing buildup of activity related to decision formation, in a manner that was direction-selective and parametrically affected by motion strength. Our results are not due to the mere presence of motion stimuli because the dependencies on coherence and directional congruency were eliminated in a single-task (saccade only) control experiment. Revealing such interactions between decision making and saccade executions suggests that these two types of signals cannot be completely demixed in neural circuitry. Meeting abstract presented at VSS 2014

The Effect of FEF Microstimulation on the Responses of Neurons in the Lateral Intraparietal Area

The macaque FEFs and the lateral intraparietal area (LIP) are high-level cortical areas involved in both spatial attention and oculomotor behavior. Stimulating FEF at a level below the threshold for evoking saccades increases fMRI activity and gamma power in area LIP, but the precise effect exerted by the FEF on LIP neurons is unknown. In our study, we recorded LIP single-unit activity during a visually guided saccade task with a peripherally presented go signal during microstimulation of FEF. We found that FEF microstimulation increased the LIP spike rate immediately after the highly salient go signal inside the LIP receptive field when both target and go signal were presented inside the receptive field, and no other possible go cues were present on the screen. The effect of FEF microstimulation on the LIP response was positive until at least 800 msec after microstimulation had ceased, but reversed for longer trial durations. Therefore, FEF microstimulation can modulate the LIP spike rate only when attention is selectively directed toward the stimulated location. These results provide the first direct evidence for LIP spike rate modulations caused by FEF microstimulation, thus showing that FEF activity can be the source of top-down control of area LIP.

Transition of target-location signaling in activity of macaque lateral intraparietal neurons during delayed-response visual search.

Neurons in the lateral intraparietal area (LIP) are involved in signaling the location of behaviorally relevant objects during visual discrimination and working memory maintenance. Although previous studies have examined these cognitive processes separately, they often appear as inseparable sequential processes in real-life situations. Little is known about how the neural representation of the target location is altered when both cognitive processes are continuously required for executing a task. We investigated this issue by recording single-unit activity from LIP of monkeys performing a delayed-response visual search task in which they were required to discriminate the target from distractors in the stimulus period, remember the location at which the extinguished target had been presented in the delay period, and make a saccade to that location in the response period. Target-location signaling was assessed using response modulations contingent on whether the target location was inside or opposite the receptive field. Although the population-averaged response modulation was consistent and changed only slightly during a trial, the across-neuron pattern of response modulations showed a marked and abrupt change around 170 ms after stimulus offset due to concurrent changes in the response modulations of a subset of LIP neurons, which manifested heterogeneous patterns of activity changes during the task. Our findings suggest that target-location signaling by the across-neuron pattern of LIP activity discretely changes after the stimulus disappearance under conditions that continuously require visual discrimination and working memory to perform a single behavioral task.

Novelty enhances visual salience independently of reward in the parietal lobe.

Novelty modulates sensory and reward processes, but it remains unknown how these effects interact, i.e., how the visual effects of novelty are related to its motivational effects. A widespread hypothesis, based on findings that novelty activates reward-related structures, is that all the effects of novelty are explained in terms of reward. According to this idea, a novel stimulus is by default assigned high reward value and hence high salience, but this salience rapidly decreases if the stimulus signals a negative outcome. Here we show that, contrary to this idea, novelty affects visual salience in the monkey lateral intraparietal area (LIP) in ways that are independent of expected reward. Monkeys viewed peripheral visual cues that were novel or familiar (received few or many exposures) and predicted whether the trial will have a positive or a negative outcome--i.e., end in a reward or a lack of reward. We used a saccade-based assay to detect whether the cues automatically attracted or repelled attention from their visual field location. We show that salience--measured in saccades and LIP responses--was enhanced by both novelty and positive reward associations, but these factors were dissociable and habituated on different timescales. The monkeys rapidly recognized that a novel stimulus signaled a negative outcome (and withheld anticipatory licking within the first few presentations), but the salience of that stimulus remained high for multiple subsequent presentations. Therefore, novelty can provide an intrinsic bonus for attention that extends beyond the first presentation and is independent of physical rewards.

A neural mechanism of speed-accuracy tradeoff in macaque area LIP.

Decision making often involves a tradeoff between speed and accuracy. Previous studies indicate that neural activity in the lateral intraparietal area (LIP) represents the gradual accumulation of evidence toward a threshold level, or evidence bound, which terminates the decision process. The level of this bound is hypothesized to mediate the speed-accuracy tradeoff. To test this, we recorded from LIP while monkeys performed a motion discrimination task in two speed-accuracy regimes. Surprisingly, the terminating threshold levels of neural activity were similar in both regimes. However, neurons recorded in the faster regime exhibited stronger evidence-independent activation from the beginning of decision formation, effectively reducing the evidence-dependent neural modulation needed for choice commitment. Our results suggest that control of speed vs accuracy may be exerted through changes in decision-related neural activity itself rather than through changes in the threshold applied to such neural activity to terminate a decision.

Inferring eye position from populations of lateral intraparietal neurons.

Understanding how the brain computes eye position is essential to unraveling high-level visual functions such as eye movement planning, coordinate transformations and stability of spatial awareness. The lateral intraparietal area (LIP) is essential for this process. However, despite decades of research, its contribution to the eye position signal remains controversial. LIP neurons have recently been reported to inaccurately represent eye position during a saccadic eye movement, and to be too slow to support a role in high-level visual functions. We addressed this issue by predicting eye position and saccade direction from the responses of populations of LIP neurons. We found that both signals were accurately predicted before, during and after a saccade. Also, the dynamics of these signals support their contribution to visual functions. These findings provide a principled understanding of the coding of information in populations of neurons within an important node of the cortical network for visual-motor behaviors.DOI: http://dx.doi.org/10.7554/eLife.02813.001.

Neural Correlates of Temporal Credit Assignment in the Parietal Lobe

Empirical studies of decision making have typically assumed that value learning is governed by time, such that a reward prediction error arising at a specific time triggers temporally-discounted learning for all preceding actions. However, in natural behavior, goals must be acquired through multiple actions, and each action can have different significance for the final outcome. As is recognized in computational research, carrying out multi-step actions requires the use of credit assignment mechanisms that focus learning on specific steps, but little is known about the neural correlates of these mechanisms. To investigate this question we recorded neurons in the monkey lateral intraparietal area (LIP) during a serial decision task where two consecutive eye movement decisions led to a final reward. The underlying decision trees were structured such that the two decisions had different relationships with the final reward, and the optimal strategy was to learn based on the final reward at one of the steps (the “F” step) but ignore changes in this reward at the remaining step (the “I” step). In two distinct contexts, the F step was either the first or the second in the sequence, controlling for effects of temporal discounting. We show that LIP neurons had the strongest value learning and strongest post-decision responses during the transition after the F step regardless of the serial position of this step. Thus, the neurons encode correlates of temporal credit assignment mechanisms that allocate learning to specific steps independently of temporal discounting.

Optogenetic and Electrical Microstimulation Systematically Bias Visuospatial Choice in Primates

Optogenetics is a recently developed method in which neurons are genetically modified to express membrane proteins sensitive to light, enabling precisely targeted control of neural activity [1-3]. The temporal and spatial precision afforded by neural stimulation by light holds promise as a powerful alternative to current methods of neural control, which rely predominantly on electrical and pharmacological methods, in both research and clinical settings [4, 5]. Although the optogenetic approach has been widely used in rodent and other small animal models to study neural circuitry [6-8], its functional application in primate models has proven more difficult. In contrast to the relatively large literature on the effects of cortical electrical microstimulation in perceptual and decision-making tasks [9-13], previous studies of optogenetic stimulation in primates have not demonstrated its utility in similar paradigms [14-18]. In this study, we directly compare the effects of optogenetic activation and electrical microstimulation in the lateral intraparietal area during a visuospatial discrimination task. We observed significant and predictable biases in visual attention in response to both forms of stimulation that are consistent with the experimental modulation of a visual salience map. Our results demonstrate the power of optogenetics as a viable alternative to electrical microstimulation for the precise dissection of the cortical pathways of high-level processes in the primate brain.

Spatially Invariant Coding of Numerical Information in Functionally Defined Subregions of Human Parietal Cortex

Macaque electrophysiology has revealed neurons responsive to number in lateral (LIP) and ventral (VIP) intraparietal areas. Recently, fMRI pattern recognition revealed information discriminative of individual numbers in human parietal cortex but without precisely localizing the relevant sites or testing for subregions with different response profiles. Here, we defined the human functional equivalents of LIP (feLIP) and VIP (feVIP) using neurophysiologically motivated localizers. We applied multivariate pattern recognition to investigate whether both regions represent numerical information and whether number codes are position specific or invariant. In a delayed number comparison paradigm with laterally presented numerosities, parietal cortex discriminated between numerosities better than early visual cortex, and discrimination generalized across hemifields in parietal, but not early visual cortex. Activation patterns in the 2 parietal regions of interest did not differ in the coding of position-specific or position-independent number information, but in the expression of a numerical distance effect which was more pronounced in feLIP. Thus, the representation of number in parietal cortex is at least partially position invariant. Both feLIP and feVIP contain information about individual numerosities in humans, but feLIP hosts a coarser representation of numerosity than feVIP, compatible with either broader tuning or a summation code.

Parietal blood oxygenation level-dependent response evoked by covert visual search reflects set-size effect in monkeys

Distinguishing a target from distractors during visual search is crucial for goal-directed behaviour. The more distractors that are presented with the target, the larger is the subject's error rate. This observation defines the set-size effect in visual search. Neurons in areas related to attention and eye movements, like the lateral intraparietal area (LIP) and frontal eye field (FEF), diminish their firing rates when the number of distractors increases, in line with the behavioural set-size effect. Furthermore, human imaging studies that have tried to delineate cortical areas modulating their blood oxygenation level-dependent (BOLD) response with set size have yielded contradictory results. In order to test whether BOLD imaging of the rhesus monkey cortex yields results consistent with the electrophysiological findings and, moreover, to clarify if additional other cortical regions beyond the two hitherto implicated are involved in this process, we studied monkeys while performing a covert visual search task. When varying the number of distractors in the search task, we observed a monotonic increase in error rates when search time was kept constant as was expected if monkeys resorted to a serial search strategy. Visual search consistently evoked robust BOLD activity in the monkey FEF and a region in the intraparietal sulcus in its lateral and middle part, probably involving area LIP. Whereas the BOLD response in the FEF did not depend on set size, the LIP signal increased in parallel with set size. These results demonstrate the virtue of BOLD imaging in monkeys when trying to delineate cortical areas underlying a cognitive process like visual search. However, they also demonstrate the caution needed when inferring neural activity from BOLD activity.

Estimates of segregation and overlap of functional connectivity networks in the human cerebral cortex

The organization of the human cerebral cortex has recently been explored using techniques for parcellating the cortex into distinct functionally coupled networks. The divergent and convergent nature of cortico-cortical anatomic connections suggests the need to consider the possibility of regions belonging to multiple networks and hierarchies among networks. Here we applied the Latent Dirichlet Allocation (LDA) model and spatial independent component analysis (ICA) to solve for functionally coupled cerebral networks without assuming that cortical regions belong to a single network. Data analyzed included 1000 subjects from the Brain Genomics Superstruct Project (GSP) and 12 high quality individual subjects from the Human Connectome Project (HCP). The organization of the cerebral cortex was similar regardless of whether a winner-take-all approach or the more relaxed constraints of LDA (or ICA) were imposed. This suggests that large-scale networks may function as partially isolated modules. Several notable interactions among networks were uncovered by the LDA analysis. Many association regions belong to at least two networks, while somatomotor and early visual cortices are especially isolated. As examples of interaction, the precuneus, lateral temporal cortex, medial prefrontal cortex and posterior parietal cortex participate in multiple paralimbic networks that together comprise subsystems of the default network. In addition, regions at or near the frontal eye field and human lateral intraparietal area homologue participate in multiple hierarchically organized networks. These observations were replicated in both datasets and could be detected (and replicated) in individual subjects from the HCP.

Evidence for differential top-down and bottom-up suppression in posterior parietal cortex

When searching for an object, we usually avoid items that are visually different from the target and objects or places that have been searched already. Previous studies have shown that neural activity in the lateral intraparietal area (LIP) can be used to guide this behaviour; responses to task irrelevant stimuli or to stimuli that have been fixated previously in the trial are reduced compared with responses to potential targets. Here, we test the hypothesis that these reduced responses have a different genesis. Two animals were trained on a visual foraging task, in which they had to find a target among a number of physically identical potential targets (T) and task irrelevant distractors. We recorded neural activity and local field potentials (LFPs) in LIP while the animals performed the task. We found that LFP power was similar for potential targets and distractors but was greater in the alpha and low beta bands when a previously fixated T was in the response field. We interpret these data to suggest that the reduced single-unit response to distractors is a bottom-up feed-forward result of processing in earlier areas and the reduced response to previously fixated Ts is a result of active top-down suppression.

Spatial Representation and Cognitive Modulation of Response Variability in the Lateral Intraparietal Area Priority Map

The lateral intraparietal area (LIP) in the macaque contains a priority-based representation of the visual scene. We previously showed that the mean spike rate of LIP neurons is strongly influenced by spatially wide-ranging surround suppression in a manner that effectively sharpens the priority map. Reducing response variability can also improve the precision of LIP's priority map. We show that when a monkey plans a visually guided delayed saccade with an intervening distractor, variability (measured by the Fano factor) decreases both for neurons representing the saccade goal and for neurons representing the broad spatial surround. The reduction in Fano factor is maximal for neurons representing the saccade goal and steadily decreases for neurons representing more distant locations. LIP Fano factor changes are behaviorally significant: increasing expected reward leads to lower variability for the LIP representation of both the target and distractor locations, and trials with shorter latency saccades are associated with lower Fano factors in neurons representing the surround. Thus, the LIP Fano factor reflects both stimulus and behavioral engagement. Quantitative modeling shows that the interaction between mean spike count and target-receptive field (RF) distance in the surround during the predistractor epoch is multiplicative: the Fano factor increases more steeply with mean spike count further away from the RF. A negative-binomial model for LIP spike counts captures these findings quantitatively, suggests underlying mechanisms based on trial-by-trial variations in mean spike rate or burst-firing patterns, and potentially provides a principled framework to account simultaneously for the previously observed unsystematic relationships between spike rate and variability in different brain areas.

Separate evaluation of target facilitation and distractor suppression in the activity of macaque lateral intraparietal neurons during visual search

During visual search, neurons in the lateral intraparietal area (LIP) discriminate the target from distractors by exhibiting stronger activation when the target appears within the receptive field than when it appears outside the receptive field. It is generally thought that such target-discriminative activity is produced by the combination of target-related facilitation and distractor-related suppression. However, little is known about how the target-discriminative activity is constituted by these two types of neural modulation. To address this issue, we recorded activity from LIP of monkeys performing a visual search task that consisted of target-present and target-absent trials. Monkeys had to make a saccade to a target in the target-present trials, whereas they had to maintain fixation in the target-absent trials, in which only distractors were presented. By introducing the activity from the latter trials as neutral activity, we were able to separate the target-discriminative activity into target-related elevation and distractor-related reduction components. We found that the target-discriminative activity of most LIP neurons consisted of the combination of target-related elevation and distractor-related reduction or only target-related elevation. In contrast, target-discriminative activity composed of only distractor-related reduction was observed for very few neurons. We also found that, on average, target-related elevation was stronger and occurred earlier compared with distractor-related reduction. Finally, we consider possible underlying mechanisms, including lateral inhibitory interactions, responsible for target-discriminative activity in visual search. The present findings provide insight into how neuronal modulations shape target-discriminative activity during visual search.

An Evaluation of the Left-Brain vs. Right-Brain Hypothesis with Resting State Functional Connectivity Magnetic Resonance Imaging

Lateralized brain regions subserve functions such as language and visuospatial processing. It has been conjectured that individuals may be left-brain dominant or right-brain dominant based on personality and cognitive style, but neuroimaging data has not provided clear evidence whether such phenotypic differences in the strength of left-dominant or right-dominant networks exist. We evaluated whether strongly lateralized connections covaried within the same individuals. Data were analyzed from publicly available resting state scans for 1011 individuals between the ages of 7 and 29. For each subject, functional lateralization was measured for each pair of 7266 regions covering the gray matter at 5-mm resolution as a difference in correlation before and after inverting images across the midsagittal plane. The difference in gray matter density between homotopic coordinates was used as a regressor to reduce the effect of structural asymmetries on functional lateralization. Nine left- and 11 right-lateralized hubs were identified as peaks in the degree map from the graph of significantly lateralized connections. The left-lateralized hubs included regions from the default mode network (medial prefrontal cortex, posterior cingulate cortex, and temporoparietal junction) and language regions (e.g., Broca Area and Wernicke Area), whereas the right-lateralized hubs included regions from the attention control network (e.g., lateral intraparietal sulcus, anterior insula, area MT, and frontal eye fields). Left- and right-lateralized hubs formed two separable networks of mutually lateralized regions. Connections involving only left- or only right-lateralized hubs showed positive correlation across subjects, but only for connections sharing a node. Lateralization of brain connections appears to be a local rather than global property of brain networks, and our data are not consistent with a whole-brain phenotype of greater “left-brained” or greater “right-brained” network strength across individuals. Small increases in lateralization with age were seen, but no differences in gender were observed.

Temporal structure in the lateral intraparietal area (LIP) neuronal activity during dynamic visual search

The ability to recognize targets from distractors is as crucial as remembering where you have looked when performing dynamic visual search. We have shown that activity in LIP encodes all these elements; the average spiking responses of LIP neurons not only differentiate between targets and distractors, but also keep track of already visited locations during visual search. It has also been shown that the power spectra of LIP activity exhibits a spatially tuned temporal structure in memory guided eye movements. However it has not been shown whether there is temporal structure in LIP activity during dynamic visual search. To address this question, we recorded local field potentials (LFPs) from LIP while two animals performed a visual foraging task. In this task, animals search through an array of 5 task irrelevant distractors and 5 Ts, one of which has a reward linked to it (the target). To obtain the reward, the animal must fixate the target for 500 ms. The stimuli are arranged such that when the animal fixates one stimulus, another is likely to be in the response field of the single neuron being recorded when the LFP was collected. We found that raw LFPs distinguished between the Ts and the irrelevant distractors in addition to new from visited objects. In the spectral analysis of the LFP, we found the temporal structure related to efficient foraging behavior. The spectral power in the mid-gamma band differentiated targets, distractors and visited objects. In addition there was an elevation of power in alpha band which appeared much earlier and was only present when an already visited object was in the receptive filed. We suggest that this signal, which may be a neural correlate of search memory, or inhibition or return, is separate from the feed-forward signal that differentiates between the stimulus classes. Meeting abstract presented at VSS 2013

Eye-Position Signals in the Dorsal Visual System Are Accurate and Precise on Short Timescales

Eye-position signals (EPS) are found throughout the primate visual system and are thought to provide a mechanism for representing spatial locations in a manner that is robust to changes in eye position. It remains unknown, however, whether cortical EPS (also known as "gain fields") have the necessary spatial and temporal characteristics to fulfill their purported computational roles. To quantify these EPS, we combined single-unit recordings in four dorsal visual areas of behaving rhesus macaques (lateral intraparietal area, ventral intraparietal area, middle temporal area, and the medial superior temporal area) with likelihood-based population-decoding techniques. The decoders used knowledge of spiking statistics to estimate eye position during fixation from a set of observed spike counts across neurons. Importantly, these samples were short in duration (100 ms) and from individual trials to mimic the real-time estimation problem faced by the brain. The results suggest that cortical EPS provide an accurate and precise representation of eye position, albeit with unequal signal fidelity across brain areas and a modest underestimation of eye eccentricity. The underestimation of eye eccentricity predicted a pattern of mislocalization that matches the errors made by human observers. In addition, we found that eccentric eye positions were associated with enhanced precision relative to the primary eye position. This predicts that positions in visual space should be represented more reliably during eccentric gaze than while looking straight ahead. Together, these results suggest that cortical eye-position signals provide a useable head-centered representation of visual space on timescales that are compatible with the duration of a typical ocular fixation.

Information processing bottlenecks in macaque posterior parietal cortex: an attentional blink?

When two brief stimuli are presented in rapid succession, our ability to attend and recognize the second stimulus is impaired if our attentional resources are devoted to processing the first. Such inability (termed the "attentional blink" in human studies) arises around 200-500ms following the onset of the first stimulus. We trained two monkeys on a delayed-match-to-sample task where both the location and orientation of two successively presented grating patches had to be matched. When the delay between the two gratings was varied, monkey's behavioral performance (d') was affected in a way that was analogous to the attentional blink in humans. Furthermore, a subset of neurons in the monkey's lateral intraparietal area, known to be crucial in the control of attention, closely followed the variation in d', even on occasions when d' followed an atypical pattern. Our results provide the first behavioral demonstration of an attentional bottleneck in the macaque of a type similar to the human attentional blink as well as a possible single-neuron correlate of the phenomenon.