LIP Neurons Research Articles

Neuronal Response to Reward and Luminance in Macaque LIP During Saccadic Choice

Recent work in decision neuroscience suggests that visual saliency can interact with reward-based choice, and the lateral intraparietal cortex (LIP) is implicated in this process. In this study, we recorded from LIP neurons while monkeys performed a two alternative choice task in which the reward and luminance associated with each offer were varied independently. We discovered that the animal’s choice was dictated by the reward amount while the luminance had a marginal effect. In the LIP, neuronal activity corresponded well with the animal’s choice pattern, in that a majority of reward-modulated neurons encoded the reward amount in the neuron’s preferred hemifield with a positive slope. In contrast, compared to their responses to low luminance, an approximately equal proportion of luminance-sensitive neurons responded to high luminance with increased or decreased activity, leading to a much weaker population-level response. Meanwhile, in the non-preferred hemifield, the strength of encoding for reward amount and luminance was positively correlated, suggesting the integration of these two factors in the LIP. Moreover, neurons encoding reward and luminance were homogeneously distributed along the anterior-posterior axis of the LIP. Overall, our study provides further evidence supporting the neural instantiation of a priority map in the LIP in reward-based decisions.

Sequential sampling from memory underlies action selection during abstract decision-making

The study of perceptual decision-making in monkeys has provided insights into the process by which sensory evidence is integrated toward a decision. When monkeys make decisions with the knowledge of the motor actions the decisions bear upon, the process of evidence integration is instantiated by neurons involved in the selection of said actions. It is less clear how monkeys make decisions when unaware of the actions required to communicate their choice-what we refer to as "abstract" decisions. We investigated this by training monkeys to associate the direction of motion of a noisy random-dot display with the color of two targets. Crucially, the targets were displayed at unpredictable locations after the motion stimulus was extinguished. We found that the monkeys postponed decision formation until the targets were revealed. Neurons in the parietal association area LIP represented the integration of evidence leading to a choice, but as the stimulus was no longer visible, the samples of evidence must have been retrieved from short-term memory. Our results imply that when decisions are temporally unyoked from the motor actions they bear upon, decision formation is protracted until they can be framed in terms of motor actions.

Coding of interceptive saccades in parietal cortex of macaque monkeys

The oculomotor system can initiate remarkably accurate saccades towards moving targets (interceptive saccades) the processing of which is still under debate. The generation of these saccades requires the oculomotor centers to have information about the motion parameters of the target that then must be extrapolated to bridge the inherent processing delays. We investigated to what degree the information about motion of a saccade target is available in the lateral intra-parietal area (area LIP) of macaque monkeys for generation of accurate interceptive saccades. When a multi-layer neural network was trained based on neural discharges from area LIP around the time of saccades towards stationary targets, it was also able to predict the end points of saccades directed towards moving targets. This prediction, however, lagged behind the actual post-saccadic position of the moving target by ~ 80 ms when the whole neuronal sample of 105 neurons was used. We further found that single neurons differentially code for the motion of the target. Selecting neurons with the strongest representation of target motion reduced this lag to ~ 30 ms which represents the position of the moving target approximately at the onset of the interceptive saccade. We conclude that—similarly to recent findings from the Superior Colliculus (Goffart et al. J Neurophysiol 118(5):2890–2901)—there is a continuum of contributions of individual LIP neurons to the accuracy of interceptive saccades. A contribution of other gaze control centers (like the cerebellum or the frontal eye field) that further increase the saccadic accuracy is, however, likely.

Recurrent circuit dynamics underlie persistent activity in the macaque frontoparietal network.

During delayed oculomotor response tasks, neurons in the lateral intraparietal area (LIP) and the frontal eye fields (FEF) exhibit persistent activity that reflects the active maintenance of behaviorally relevant information. Despite many computational models of the mechanisms of persistent activity, there is a lack of circuit-level data from the primate to inform the theories. To fill this gap, we simultaneously recorded ensembles of neurons in both LIP and FEF while macaques performed a memory-guided saccade task. A population encoding model revealed strong and symmetric long-timescale recurrent excitation between LIP and FEF. Unexpectedly, LIP exhibited stronger local functional connectivity than FEF, and many neurons in LIP had longer network and intrinsic timescales. The differences in connectivity could be explained by the strength of recurrent dynamics in attractor networks. These findings reveal reciprocal multi-area circuit dynamics in the frontoparietal network during persistent activity and lay the groundwork for quantitative comparisons to theoretical models.

Discrete Stepping and Nonlinear Ramping Dynamics Underlie Spiking Responses of LIP Neurons during Decision-Making

Neurons in LIP exhibit ramping trial-averaged responses during decision-making. Recent work sparked debate over whether single-trial LIP spike trains are better described by discrete "stepping" or continuous "ramping" dynamics. We extended latent dynamical spike train models and used Bayesian model comparison to address this controversy. First, we incorporated non-Poisson spiking into both models and found that more neurons were better described by stepping than ramping, even when conditioned on evidence or choice. Second, we extended the ramping model to include a non-zero baseline and compressive output nonlinearity. This model accounted for roughly as many neurons as the stepping model. However, latent dynamics inferred under this model exhibited high diffusion variance for many neurons, softening the distinction between continuous and discrete dynamics. Results generalized to additional datasets, demonstrating that substantial fractions of neurons are well described by either stepping or nonlinear ramping, which may be less categorically distinct than the original labels implied.

Responses of Neurons in Lateral Intraparietal Area Depend on Stimulus-Associated Reward During Binocular Flash Suppression.

Discovering neural correlates of subjective perception and dissociating them from sensory input has fascinated neuroscientists for a long time. Bistable and multistable perception phenomena have exhibited great experimental potential to address this question. Here, we performed electrophysiological recordings from single neurons in lateral intraparietal area (LIP) of rhesus macaques during stimulus and perceptual transitions induced by binocular flash suppression (BFS). LIP neurons demonstrated transient bursts of activity after stimulus presentation and stimulus or perceptual switches but only a minority of cells demonstrated stimulus and perceptual selectivity. To enhance LIP neural selectivity, we performed a second experiment in which the competing stimuli were associated with asymmetric rewards. We found that transient and sustained activities substantially increased while the proportion of stimulus selective neurons remained approximately the same, albeit with increased selectivity magnitude. In addition, we observed mild increases in the proportion of perceptually selective neurons which also showed increase magnitude of selectivity. Importantly, the increased selectivity of cells after the reward manipulation was not directly reflecting the reward size per se but an enhancement in stimulus differentiation. Based on our results, we conjecture that LIP contributes to perceptual transitions and serves a modulatory role in perceptual selection taking into account the stimulus behavioral value.

Sub-millimeter fMRI Reveals Columnar Organization in Macaque Parietal Cortex

Sub-millimeter fMRI Reveals Columnar Organization in Macaque Parietal Cortex

Distinct roles of prefrontal and parietal areas in the encoding of attentional priority

When searching for an object in a crowded scene, information about the similarity of stimuli to the target object is thought to be encoded in spatial priority maps, which are subsequently used to guide shifts of attention and gaze to likely targets. Two key cortical areas that have been described as holding priority maps are the frontal eye field (FEF) and the lateral intraparietal area (LIP). However, little is known about their distinct contributions in priority encoding. Here, we compared neuronal responses in FEF and LIP during free-viewing visual search. Although saccade selection signals emerged earlier in FEF, information about the target emerged at similar latencies in distinct populations within the two areas. Notably, however, effects in FEF were more pronounced. Moreover, LIP neurons encoded the similarity of stimuli to the target independent of saccade selection, whereas in FEF, encoding of target similarity was strongly modulated by saccade selection. Taken together, our findings suggest hierarchical processing of saccade selection signals and parallel processing of feature-based attention signals within the parietofrontal network with FEF having a more prominent role in priority encoding. Furthermore, they suggest discrete roles of FEF and LIP in the construction of priority maps.

The effect of context on sensory accumulation involved in decision-making

The underlying processes allowing for decision-making has been a question of interest for many neuroscientists. The lateral intraparietal cortex, or LIP, was shown to accumulate context and sensory information to compute a decision variable. The following review will present the work of Kumano, Suda and Uka who studied the link between context and sensory information during decision-making. To do so, a monkey was trained to associate the color of a fixating dot to one of two tasks. The tasks consisted in either indicating the motion or the depth of themajority of the dots on a screen. The local field potential of the LIP neurons was recorded, and the researchers found a role of context during the stimulus presentation in regards to decision formation. The results have important implication for mental disorders involving malfunction in decision processes.

Learning Peri-saccadic Remapping of Receptive Field from Experience in Lateral Intraparietal Area.

Our eyes move constantly at a frequency of 3–5 times per second. These movements, called saccades, induce the sweeping of visual images on the retina, yet we perceive the world as stable. It has been suggested that the brain achieves this visual stability via predictive remapping of neuronal receptive field (RF). A recent experimental study disclosed details of this remapping process in the lateral intraparietal area (LIP), that is, about the time of the saccade, the neuronal RF expands along the saccadic trajectory temporally, covering the current RF (CRF), the future RF (FRF), and the region the eye will sweep through during the saccade. A cortical wave (CW) model was also proposed, which attributes the RF remapping as a consequence of neural activity propagating in the cortex, triggered jointly by a visual stimulus and the corollary discharge (CD) signal responsible for the saccade. In this study, we investigate how this CW model is learned naturally from visual experiences at the development of the brain. We build a two-layer network, with one layer consisting of LIP neurons and the other superior colliculus (SC) neurons. Initially, neuronal connections are random and non-selective. A saccade will cause a static visual image to sweep through the retina passively, creating the effect of the visual stimulus moving in the opposite direction of the saccade. According to the spiking-time-dependent-plasticity rule, the connection path in the opposite direction of the saccade between LIP neurons and the connection path from SC to LIP are enhanced. Over many such visual experiences, the CW model is developed, which generates the peri-saccadic RF remapping in LIP as observed in the experiment.

Coding of spatial attention priorities and object features in the macaque lateral intraparietal cortex.

Primate posterior parietal cortex (PPC) is known to be involved in controlling spatial attention. Neurons in one part of the PPC, the lateral intraparietal area (LIP), show enhanced responses to objects at attended locations. Although many are selective for object features, such as the orientation of a visual stimulus, it is not clear how LIP circuits integrate feature‐selective information when providing attentional feedback about behaviorally relevant locations to the visual cortex. We studied the relationship between object feature and spatial attention properties of LIP cells in two macaques by measuring the cells' orientation selectivity and the degree of attentional enhancement while performing a delayed match‐to‐sample task. Monkeys had to match both the location and orientation of two visual gratings presented separately in time. We found a wide range in orientation selectivity and degree of attentional enhancement among LIP neurons. However, cells with significant attentional enhancement had much less orientation selectivity in their response than cells which showed no significant modulation by attention. Additionally, orientation‐selective cells showed working memory activity for their preferred orientation, whereas cells showing attentional enhancement also synchronized with local neuronal activity. These results are consistent with models of selective attention incorporating two stages, where an initial feature‐selective process guides a second stage of focal spatial attention. We suggest that LIP contributes to both stages, where the first stage involves orientation‐selective LIP cells that support working memory of the relevant feature, and the second stage involves attention‐enhanced LIP cells that synchronize to provide feedback on spatial priorities.

Computing by Robust Transience: How the Fronto-Parietal Network Performs Sequential, Category-Based Decisions

Decision making involves dynamic interplay between internal judgements and external perception, which has been investigated in delayed match-to-category (DMC) experiments. Our analysis of neural recordings shows that, during DMC tasks, LIP and PFC neurons demonstrate mixed, time-varying, and heterogeneous selectivity, but previous theoretical work has not established the link between these neural characteristics and population-level computations. We trained a recurrent network model to perform DMC tasks and found that the model can remarkably reproduce key features of neuronal selectivity at the single-neuron and population levels. Analysis of the trained networks elucidates that robust transient trajectories of the neural population are the key driver of sequential categorical decisions. The directions of trajectories are governed by network self-organized connectivity, defining a "neural landscape" consisting of a task-tailored arrangement of slow states and dynamical tunnels. With this model, we can identify functionally relevant circuit motifs and generalize the framework to solve other categorization tasks.

Context-Dependent Accumulation of Sensory Evidence in the Parietal Cortex Underlies Flexible Task Switching.

Flexible behavior depending on context is a hallmark of human cognition. During flexible behavior, the frontal and parietal cortices have complex representations that hinder efforts to conceptualize their underlying computations. We now provide evidence that neurons in the lateral intraparietal area accumulate relevant information preferentially depending on context. We suggest that behavioral flexibility is implemented in the form of temporal integration gain control in the parietal cortex.

Two subdivisions of macaque LIP process visual-oculomotor information differently

Although the cerebral cortex is thought to be composed of functionally distinct areas, the actual parcellation of area and assignment of function are still highly controversial. An example is the much-studied lateral intraparietal cortex (LIP). Despite the general agreement that LIP plays an important role in visual-oculomotor transformation, it remains unclear whether the area is primary sensory- or motor-related (the attention-intention debate). Although LIP has been considered as a functionally unitary area, its dorsal (LIPd) and ventral (LIPv) parts differ in local morphology and long-distance connectivity. In particular, LIPv has much stronger connections with two oculomotor centers, the frontal eye field and the deep layers of the superior colliculus, than does LIPd. Such anatomical distinctions imply that compared with LIPd, LIPv might be more involved in oculomotor processing. We tested this hypothesis physiologically with a memory saccade task and a gap saccade task. We found that LIP neurons with persistent memory activities in memory saccade are primarily provoked either by visual stimulation (vision-related) or by both visual and saccadic events (vision-saccade-related) in gap saccade. The distribution changes from predominantly vision-related to predominantly vision-saccade-related as the recording depth increases along the dorsal-ventral dimension. Consistently, the simultaneously recorded local field potential also changes from visual evoked to saccade evoked. Finally, local injection of muscimol (GABA agonist) in LIPv, but not in LIPd, dramatically decreases the proportion of express saccades. With these results, we conclude that LIPd and LIPv are more involved in visual and visual-saccadic processing, respectively.

Decision Activity in Parietal Cortex – Leader or Follower?

Katz and colleagues demonstrate that inactivating the primate lateral intraparietal area (LIP) spares visual motion decisions, even though these same decisions strongly modulate LIP neurons. This work is the latest addition to an intense effort spanning sensory modalities, animals, and techniques to understand which structures comprise the circuits responsible for interpreting sensory signals to make decisions.

The effects of short-term and long-term learning on the responses of lateral intraparietal neurons to visually presented objects.

The lateral intraparietal area (LIP) is thought to play an important role in the guidance of where to look and pay attention. LIP can also respond selectively to differently shaped objects. We sought to understand to what extent short-term and long-term experience with visual orienting determines the responses of LIP to objects of different shapes. We taught monkeys to arbitrarily associate centrally presented objects of various shapes with orienting either toward or away from a preferred spatial location of a neuron. The training could last for less than a single day or for several months. We found that neural responses to objects are affected by such experience, but that the length of the learning period determines how this neural plasticity manifests. Short-term learning affects neural responses to objects, but these effects are only seen relatively late after visual onset; at this time, the responses to newly learned objects resemble those of familiar objects that share their meaning or arbitrary association. Long-term learning affects the earliest bottom-up responses to visual objects. These responses tend to be greater for objects that have been associated with looking toward, rather than away from, LIP neurons' preferred spatial locations. Responses to objects can nonetheless be distinct, although they have been similarly acted on in the past and will lead to the same orienting behavior in the future. Our results therefore indicate that a complete experience-driven override of LIP object responses may be difficult or impossible. We relate these results to behavioral work on visual attention.

A Neural Model of Distance-Dependent Percept of Object Size Constancy.

Size constancy is one of the well-known visual phenomena that demonstrates perceptual stability to account for the effect of viewing distance on retinal image size. Although theories involving distance scaling to achieve size constancy have flourished based on psychophysical studies, its underlying neural mechanisms remain unknown. Single cell recordings show that distance-dependent size tuned cells are common along the ventral stream, originating from V1, V2, and V4 leading to IT. In addition, recent research employing fMRI demonstrates that an object’s perceived size, associated with its perceived egocentric distance, modulates its retinotopic representation in V1. These results suggest that V1 contributes to size constancy, and its activity is possibly regulated by feedback of distance information from other brain areas. Here, we propose a neural model based on these findings. First, we construct an egocentric distance map in LIP by integrating horizontal disparity and vergence through gain-modulated MT neurons. Second, LIP neurons send modulatory feedback of distance information to size tuned cells in V1, resulting in a spread of V1 cortical activity. This process provides V1 with distance-dependent size representations. The model supports that size constancy is preserved by scaling retinal image size to compensate for changes in perceived distance, and suggests a possible neural circuit capable of implementing this process.

Reward-based decision signals in parietal cortex are partially embodied.

Recordings in the lateral intraparietal area (LIP) reveal that parietal cortex encodes variables related to spatial decision-making, the selection of desirable targets in space. It has been unclear whether parietal cortex is involved in spatial decision-making in general, or whether specific parietal compartments subserve decisions made using specific actions. To test this, we engaged monkeys (Macaca mulatta) in a reward-based decision task in which they selected a target based on its desirability. The animals' choice behavior in this task followed the molar matching law, and in each trial was governed by the desirability of the choice targets. Critically, animals were instructed to make the choice using one of two actions: eye movements (saccades) and arm movements (reaches). We recorded the discharge activity of neurons in area LIP and the parietal reach region (PRR) of the parietal cortex. In line with previous studies, we found that both LIP and PRR encode a reward-based decision variable, the target desirability. Crucially, the target desirability was encoded in LIP at least twice as strongly when choices were made using saccades compared with reaches. In contrast, PRR encoded target desirability only for reaches and not for saccades. These data suggest that decisions can evolve in dedicated parietal circuits in the context of specific actions. This finding supports the hypothesis of an intentional representation of developing decisions in parietal cortex. Furthermore, the close link between the cognitive (decision-related) and bodily (action-related) processes presents a neural contribution to the theories of embodied cognition.

Region-Specific Summation Patterns Inform the Role of Cortical Areas in Selecting Motor Plans.

Given an instruction regarding which effector to move and what location to move to, simply adding the effector and spatial signals together will not lead to movement selection. For this, a nonlinearity is required. Thresholds, for example, can be used to select a particular response and reject others. Here we consider another useful nonlinearity, a supralinear multiplicative interaction. To help select a motor plan, spatial and effector signals could multiply and thereby amplify each other. Such an amplification could constitute one step within a distributed network involved in response selection, effectively boosting one response while suppressing others. We therefore asked whether effector and spatial signals sum supralinearly for planning eye versus arm movements from the parietal reach region (PRR), the lateral intraparietal area (LIP), the frontal eye field (FEF), and a portion of area 5 (A5) lying just anterior to PRR. Unlike LIP neurons, PRR, FEF, and, to a lesser extent, A5 neurons show a supralinear interaction. Our results suggest that selecting visually guided eye versus arm movements is likely to be mediated by PRR and FEF but not LIP.

Representation of accumulating evidence for a decision in two parietal areas.

Decisions are often made by accumulating evidence for and against the alternatives. The momentary evidence represented by sensory neurons is accumulated by downstream structures to form a decision variable, linking the evolving decision to the formation of a motor plan. When decisions are communicated by eye movements, neurons in the lateral intraparietal area (LIP) represent the accumulation of evidence bearing on the potential targets for saccades. We now show that reach-related neurons from the medial intraparietal area (MIP) exhibit a gradual modulation of their firing rates consistent with the representation of an evolving decision variable. When decisions were communicated by saccades instead of reaches, decision-related activity was attenuated in MIP, whereas LIP neurons were active while monkeys communicated decisions by saccades or reaches. Thus, for decisions communicated by a hand movement, a parallel flow of sensory information is directed to parietal areas MIP and LIP during decision formation.