Lateral Intraparietal Neurons Research Articles

Dissociable neuronal substrates of visual feature attention and working memory

Attention and working memory (WM) are distinct cognitive functions, yet given their close interactions, it is often assumed that they share the same neuronal mechanisms. We show that in macaques performing a WM-guided feature attention task, the activity of most neurons in areas middle temporal (MT), medial superior temporal (MST), lateral intraparietal (LIP), and posterior lateral prefrontal cortex (LPFC-p) displays attentional modulation or WM coding and not both. One area thought to play a role in both functions is LPFC-p. Totest this, we optogenetically inactivated LPFC-p bilaterally during different task periods. Attention periodinactivation reduced attentional modulation in LPFC-p, MST, and LIP neurons and impaired task performance. In contrast, WM period inactivation did not affect attentional modulation or performance and minimally affected WM coding. Our results suggest that feature attention and WM have dissociable neuronal substrates and that LPFC-p plays a critical role in feature attention, but not in WM.

Neuronal activity in posterior parietal cortex area LIP is not sufficient for saccadic eye movement production

It is widely recognized that the posterior parietal cortex (PPC) plays a role in active exploration with eye movements, arm reaching, and hand grasping. Whether this role is causal in nature is largely unresolved. One region of the PPC appears dedicated to the control of saccadic eye movement—lateral intraparietal (LIP) area. This area LIP possesses direct projections to well-established oculomotor centers and contains neurons with movement-related activity. In this study, we tested whether these neurons are implicated in saccade initiation and production. The movement-related activity of LIP neurons was tested by recording these neurons while monkeys performed a countermanding task. We found that LIP neuronal activity is not different before the execution or the cancelation of commanded saccades and thereby is not sufficient for the initiation and production of saccades. Consistent with the evolutionarily late emergence of the PPC, this finding relegates the role of this PPC area to processes that can regulate but not trigger eye movements.

Neuronal Correlates of Many-To-One Sensorimotor Mapping in Lateral Intraparietal Cortex.

Efficiently mapping sensory stimuli onto motor programs is crucial for rapidly choosing appropriate behavioral responses. While neuronal mechanisms underlying simple, one-to-one sensorimotor mapping have been extensively studied, how the brain achieves complex, many-to-one sensorimotor mapping remains unclear. Here, we recorded single neuron activity from the lateral intraparietal (LIP) cortex of monkeys trained to map multiple spatial positions of visual cue onto two opposite saccades. We found that LIP neurons' activity was consistent with directly mapping multiple cue positions to the associated saccadic direction (SDir) regardless of whether the visual cue appeared in or outside neurons' receptive fields. Unlike the explicit encoding of the visual categories, such cue-target mapping (CTM)-related activity covaried with the associated SDirs. Furthermore, the CTM was preferentially mediated by visual neurons identified by memory-guided saccade. These results indicate that LIP plays a crucial role in the early stage of many-to-one sensorimotor transformation.

In monkeys making value-based decisions, amygdala neurons are sensitive to cue value as distinct from cue salience.

Neurons in the lateral intraparietal (LIP) area of macaque monkey parietal cortex respond to cues predicting rewards and penalties of variable size in a manner that depends on the motivational salience of the predicted outcome (strong for both large reward and large penalty) rather than on its value (positive for large reward and negative for large penalty). This finding suggests that LIP mediates the capture of attention by salient events and does not encode value in the service of value-based decision making. It leaves open the question whether neurons elsewhere in the brain encode value in the identical task. To resolve this issue, we recorded neuronal activity in the amygdala in the context of the task employed in the LIP study. We found that responses to reward-predicting cues were similar between areas, with the majority of reward-sensitive neurons responding more strongly to cues that predicted large reward than to those that predicted small reward. Responses to penalty-predicting cues were, however, markedly different. In the amygdala, unlike LIP, few neurons were sensitive to penalty size, few penalty-sensitive neurons favored large over small penalty, and the dependence of firing rate on penalty size was negatively correlated with its dependence on reward size. These results indicate that amygdala neurons encoded cue value under circumstances in which LIP neurons exhibited sensitivity to motivational salience. However, the representation of negative value, as reflected in sensitivity to penalty size, was weaker than the representation of positive value, as reflected in sensitivity to reward size.NEW & NOTEWORTHY This is the first study to characterize amygdala neuronal responses to cues predicting rewards and penalties of variable size in monkeys making value-based choices. Manipulating reward and penalty size allowed distinguishing activity dependent on motivational salience from activity dependent on value. This approach revealed in a previous study that neurons of the lateral intraparietal (LIP) area encode motivational salience. Here, it reveals that amygdala neurons encode value. The results establish a sharp functional distinction between the two areas.

Neuronal pattern separation of motion-relevant input in LIP activity.

In various regions of the brain, neurons discriminate sensory stimuli by decreasing the similarity between ambiguous input patterns. Here, we examine whether this process of pattern separation may drive the rapid discrimination of visual motion stimuli in the lateral intraparietal area (LIP). Starting with a simple mean-rate population model that captures neuronal activity in LIP, we show that overlapping input patterns can be reformatted dynamically to give rise to separated patterns of neuronal activity. The population model predicts that a key ingredient of pattern separation is the presence of heterogeneity in the response of individual units. Furthermore, the model proposes that pattern separation relies on heterogeneity in the temporal dynamics of neural activity and not merely in the mean firing rates of individual neurons over time. We confirm these predictions in recordings of macaque LIP neurons and show that the accuracy of pattern separation is a strong predictor of behavioral performance. Overall, results propose that LIP relies on neuronal pattern separation to facilitate decision-relevant discrimination of sensory stimuli.NEW & NOTEWORTHY A new hypothesis is proposed on the role of the lateral intraparietal (LIP) region of cortex during rapid decision making. This hypothesis suggests that LIP alters the representation of ambiguous inputs to reduce their overlap, thus improving sensory discrimination. A combination of computational modeling, theoretical analysis, and electrophysiological data shows that the pattern separation hypothesis links neural activity to behavior and offers novel predictions on the role of LIP during sensory discrimination.

Interaction between Spatial and Feature Attention in Posterior Parietal Cortex

Lateral intraparietal (LIP) neurons encode a vast array of sensory and cognitive variables. Recently, we proposed that the flexibility of feature representations in LIP reflect the bottom-up integration of sensory signals, modulated by feature-based attention (FBA), from upstream feature-selective cortical neurons. Moreover, LIP activity is also strongly modulated by the position of space-based attention (SBA). However, the mechanisms by which SBA and FBA interact to facilitate the representation of task-relevant spatial and non-spatial features in LIP remain unclear. We recorded from LIP neurons during performance of a task that required monkeys to detect specific conjunctions of color, motion direction, and stimulus position. Here we show that FBA and SBA potentiate each other's effect in a manner consistent with attention gating the flow of visual information along the cortical visual pathway. Our results suggest that linear bottom-up integrative mechanisms allow LIP neurons to emphasize task-relevant spatial and non-spatial features.

NEURONAL MODELING. Single-trial spike trains in parietal cortex reveal discrete steps during decision-making.

Neurons in the macaque lateral intraparietal (LIP) area exhibit firing rates that appear to ramp upward or downward during decision-making. These ramps are commonly assumed to reflect the gradual accumulation of evidence toward a decision threshold. However, the ramping in trial-averaged responses could instead arise from instantaneous jumps at different times on different trials. We examined single-trial responses in LIP using statistical methods for fitting and comparing latent dynamical spike-train models. We compared models with latent spike rates governed by either continuous diffusion-to-bound dynamics or discrete "stepping" dynamics. Roughly three-quarters of the choice-selective neurons we recorded were better described by the stepping model. Moreover, the inferred steps carried more information about the animal's choice than spike counts.

A better way to explain neuronal activity

Neuronal Modeling A brain region called the lateral intraparietal (LIP) area is involved in primate decision-making. The dominant model to explain neuronal firing in LIP assumes that neurons slowly accumulate sensory evidence in favor of one choice or another. Latimer et al. hypothesized that neurons instead exhibit rapid steps or jumps in their firing rate, reflecting discrete changes in the animal's decision state. They recorded from LIP neurons in macaque monkeys performing a motion-discrimination task. LIP spike trains in most cells involved discrete stepping dynamics rather than slow evidence integration dynamics. Science , this issue p. [184][1] [1]: /lookup/doi/10.1126/science.aaa4056

In monkeys making value-based decisions, LIP neurons encode cue salience and not action value.

In monkeys deciding between alternative saccadic eye movements, lateral intraparietal (LIP) neurons representing each saccade fire at a rate proportional to the value of the reward expected upon its completion. This observation has been interpreted as indicating that LIP neurons encode saccadic value and that they mediate value-based decisions between saccades. Here, we show that LIP neurons representing a given saccade fire strongly not only if it will yield a large reward but also if it will incur a large penalty. This finding indicates that LIP neurons are sensitive to the motivational salience of cues. It is compatible neither with the idea that LIP neurons represent action value nor with the idea that value-based decisions take place in LIP neurons.

Attentional priority of saccade goal selection during visual search is represented by the relative normalized responses of lateral intraparietal neurons

Attentional priority of saccade goal selection during visual search is represented by the relative normalized responses of lateral intraparietal neurons

One-dimensional dynamics of associative representations in lateral intraparietal (LIP) area

One-dimensional dynamics of associative representations in lateral intraparietal (LIP) area

Reply to Balan and Gottlieb

REPLY: Several important questions are raised in the recent comparison by Balan and Gottlieb (2009) between the description by Balan et al. (2008) of lateral intraparietal (LIP) neuron activity in monkeys performing visual search with manual responses and our recent report of frontal eye field (FEF) neuron activity in monkeys performing visual search with saccade responses (Cohen et al. 2009). Both studies manipulated the number of distractors in the search display. Balan et al. 2008 reported decreased firing rate with increasing set size, but they reported no delay in the time at which activity for the target exceeded activity for the distractors, referred to as target selection time. Cohen and colleagues (2009) also reported decreased firing rate with increasing set size, but also observed delayed target selection time with increasing set size. How should we interpret the different observations across laboratories, effectors, cortical areas, and task designs? First, we emphasize that this is not a case of one observation being correct and the other incorrect. The results of both studies are valid within their respective contexts. However, the question remains: which difference between studies explains the different outcomes? We argue that task demands are the major factors. In other words, measured under the same task demands, we predict that the same pattern of results would be obtained across effector (manual response vs. saccade) and cortical area (LIP vs. FEF). The first step of the argument is to appreciate that categorical statements about the relationship between target selection time and response time are not possible because these times vary for at least three reasons. First, neuron type matters. Multiple

Separate Representations of Target and Timing Cue Locations in the Supplementary Eye Fields

When different stimuli indicate where and when to make an eye movement, the brain areas involved in oculomotor control must selectively plan an eye movement to the stimulus that encodes the target position and also encode the information available from the timing cue. This could pose a challenge to the oculomotor system since the representation of the timing stimulus location in one brain area might be interpreted by downstream neurons as a competing motor plan. Evidence from diverse sources has suggested that the supplementary eye fields (SEF) play an important role in behavioral timing, so we recorded single-unit activity from SEF to characterize how target and timing cues are encoded in this region. Two monkeys performed a variant of the memory-guided saccade task, in which a timing stimulus was presented at a randomly chosen eccentric location. Many spatially tuned SEF neurons encoded only the location of the target and not the timing stimulus, whereas several other SEF neurons encoded the location of the timing stimulus and not the target. The SEF population therefore encoded the location of each stimulus with largely distinct neuronal subpopulations. For comparison, we recorded a small population of lateral intraparietal (LIP) neurons in the same task. We found that most LIP neurons that encoded the location of the target also encoded the location of the timing stimulus after its presentation, but selectively encoded the intended eye movement plan in advance of saccade initiation. These results suggest that SEF, by conditionally encoding the location of instructional stimuli depending on their meaning, can help identify which movement plan represented in other oculomotor structures, such as LIP, should be selected for the next eye movement.

Coding of Shape and Position in Macaque Lateral Intraparietal Area

The analysis of object shape is critical for both object recognition and grasping. Areas in the intraparietal sulcus of the rhesus monkey are important for the visuomotor transformations underlying actions directed toward objects. The lateral intraparietal (LIP) area has strong anatomical connections with the anterior intraparietal area, which is known to control the shaping of the hand during grasping, and LIP neurons can respond selectively to simple two-dimensional shapes. Here we investigate the shape representation in area LIP of awake rhesus monkeys. Specifically, we determined to what extent LIP neurons are tuned to shape dimensions known to be relevant for grasping and assessed the invariance of their shape preferences with regard to changes in stimulus size and position in the receptive field. Most LIP neurons proved to be significantly tuned to multiple shape dimensions. The population of LIP neurons that were tested showed barely significant size invariance. Position invariance was present in a minority of the neurons tested. Many LIP neurons displayed spurious shape selectivity arising from accidental interactions between the stimulus and the receptive field. We observed pronounced differences in the receptive field profiles determined by presenting two different shapes. Almost all LIP neurons showed spatially selective saccadic activity, but the receptive field for saccades did not always correspond to the receptive field as determined using shapes. Our results demonstrate that a subpopulation of LIP neurons encodes stimulus shape. Furthermore, the shape representation in the dorsal visual stream appears to differ radically from the known representation of shape in the ventral visual stream.

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.

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.

Comparison of cortico-cortical and cortico-collicular signals for the generation of saccadic eye movements.

Many neurons in the frontal eye field (FEF) and lateral intraparietal (LIP) areas of cerebral cortex are active during the visual-motor events preceding the initiation of saccadic eye movements: they respond to visual targets, increase their activity before saccades, and maintain their activity during intervening delay periods. Previous experiments have shown that the output neurons from both LIP and FEF convey the full range of these activities to the superior colliculus (SC) in the brain stem. These areas of cerebral cortex also have strong interconnections, but what signals they convey remains unknown. To determine what these cortico-cortical signals are, we identified the LIP neurons that project to FEF by antidromic activation, and we studied their activity during a delayed-saccade task. We then compared these cortico-cortical signals to those sent subcortically by also identifying the LIP neurons that project to the intermediate layers of the SC. Of 329 FEF projection neurons and 120 SC projection neurons, none were co-activated by both FEF and SC stimulation. FEF projection neurons were encountered more superficially in LIP than SC projection neurons, which is consistent with the anatomical projection of many cortical layer III neurons to other cortical areas and of layer V neurons to subcortical structures. The estimated conduction velocities of FEF projection neurons (16.7 m/s) were significantly slower that those of SC projection neurons (21.7 m/s), indicating that FEF projection neurons have smaller axons. We identified three main differences in the discharge properties of FEF and SC projection neurons: only 44% of the FEF projection neurons changed their activity during the delayed-saccade task compared with 69% of the SC projection neurons; only 17% of the task-related FEF projection neurons showed saccadic activity, whereas 42% of the SC projection neurons showed such increases; 78% of the FEF projection neurons had a visual response but no saccadic activity, whereas only 55% of the SC projection neurons had similar activity. The FEF and SC projection neurons had three similarities: both had visual, delay, and saccadic activity, both had stronger delay and saccadic activity with visually guided than with memory-guided saccades, and both had broadly tuned responses for disparity stimuli, suggesting that their visual receptive fields have a three-dimensional configuration. These observations indicate that the activity carried between parietal and frontal cortical areas conveys a spectrum of signals but that the preponderance of activity conveyed might be more closely related to earlier visual processing than to the later saccadic stages that are directed to the SC.