LIP Neurons Research Articles

Coding dichotomy in lateral intraparietal cortex (LIP) of the macaque monkey and its role in spatial attention

Event Abstract Back to Event Coding dichotomy in lateral intraparietal cortex (LIP) of the macaque monkey and its role in spatial attention Trichur Vidyasagar1*, Ekaterina Levichkina1 and Yuri Saalmann2 1 University of Melbourne, Optometry & Vision Sciences, Australia 2 University of Wisconsin – Madison, Psychology, United States Introduction: Lateral intraparietal cortex (LIP), a part of posterior parietal cortex, is known to be involved in top-down modulation of responses to visual stimuli at earlier stages of the visual pathway1. Many of its neurons show enhancement of responses for stimuli at attended locations and many also show selectivity to the stimulus orientation1. We investigated whether there is a relationship between these two properties in LIP cells, since it has important implications for models of selective attention and the binding problem2. Methods: Two macaques were trained on a delayed match to sample task. They had to match both the location and orientation of two gratings presented with 800 ms delay between them. We measured orientation selectivity of 56 cells in LIP and also the degree of the attentional enhancement in both correct and error trials. Results: Orientation selectivity and attentional enhancement both varied considerably between LIP neurons. However, the cells (N = 25) with significant attentional enhancement (ratio of response to the second presentation of a stimulus at the same location as the first to that of the response to the first stimulus) have significantly lower orientation selectivity (Wilcoxon T-test, p<0.05). Furthermore, the population of attention-selective cells showed around 35% enhancement in correct match trials but only 27% in error trials (Wilcoxon T-test, for the group of 16 cells from sessions with sufficient errors, p<0.05). Conclusion: The results indicate that LIP may be a priority map where salient or preferred spatial locations are selected for further processing, but consequent to a first stage of selection that is sensitive to feature-sensitive inputs. Such an attentional mechanism is ideally suited for detecting targets as in the 2-stage Guided Search model2,3. 1Saalmann YB et al. (2007) Science, 316:1625. 2Vidyasagar TR (1999) Brain Res Rev., 30,66. 3Wolfe JM (1994) Psychonomic Bull. 15, 419. Keywords: macaque, spatial attention, parietal cortex, feature selectivity, guided search Conference: XII International Conference on Cognitive Neuroscience (ICON-XII), Brisbane, Queensland, Australia, 27 Jul - 31 Jul, 2014. Presentation Type: Poster Topic: Attention Citation: Vidyasagar T, Levichkina E and Saalmann Y (2015). Coding dichotomy in lateral intraparietal cortex (LIP) of the macaque monkey and its role in spatial attention. Conference Abstract: XII International Conference on Cognitive Neuroscience (ICON-XII). doi: 10.3389/conf.fnhum.2015.217.00381 Copyright: The abstracts in this collection have not been subject to any Frontiers peer review or checks, and are not endorsed by Frontiers. They are made available through the Frontiers publishing platform as a service to conference organizers and presenters. The copyright in the individual abstracts is owned by the author of each abstract or his/her employer unless otherwise stated. Each abstract, as well as the collection of abstracts, are published under a Creative Commons CC-BY 4.0 (attribution) licence (https://creativecommons.org/licenses/by/4.0/) and may thus be reproduced, translated, adapted and be the subject of derivative works provided the authors and Frontiers are attributed. For Frontiers’ terms and conditions please see https://www.frontiersin.org/legal/terms-and-conditions. Received: 19 Feb 2015; Published Online: 24 Apr 2015. * Correspondence: Prof. Trichur Vidyasagar, University of Melbourne, Optometry & Vision Sciences, Melbourne, Australia, trv@unimelb.edu.au Login Required This action requires you to be registered with Frontiers and logged in. To register or login click here. Abstract Info Abstract The Authors in Frontiers Trichur Vidyasagar Ekaterina Levichkina Yuri Saalmann Google Trichur Vidyasagar Ekaterina Levichkina Yuri Saalmann Google Scholar Trichur Vidyasagar Ekaterina Levichkina Yuri Saalmann PubMed Trichur Vidyasagar Ekaterina Levichkina Yuri Saalmann Related Article in Frontiers Google Scholar PubMed Abstract Close Back to top Javascript is disabled. Please enable Javascript in your browser settings in order to see all the content on this page.

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.

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.

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.

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.

Atoh1-dependent rhombic lip neurons are required for temporal delay between independent respiratory oscillators in embryonic mice.

All motor behaviors require precise temporal coordination of different muscle groups. Breathing, for example, involves the sequential activation of numerous muscles hypothesized to be driven by a primary respiratory oscillator, the preBötzinger Complex, and at least one other as-yet unidentified rhythmogenic population. We tested the roles of Atoh1-, Phox2b-, and Dbx1-derived neurons (three groups that have known roles in respiration) in the generation and coordination of respiratory output. We found that Dbx1-derived neurons are necessary for all respiratory behaviors, whereas independent but coupled respiratory rhythms persist from at least three different motor pools after eliminating or silencing Phox2b- or Atoh1-expressing hindbrain neurons. Without Atoh1 neurons, however, the motor pools become temporally disorganized and coupling between independent respiratory oscillators decreases. We propose Atoh1 neurons tune the sequential activation of independent oscillators essential for the fine control of different muscles during breathing.DOI: http://dx.doi.org/10.7554/eLife.02265.001.

Recovering stimulus locations using populations of eye-position modulated neurons in dorsal and ventral visual streams of non-human primates

We recorded visual responses while monkeys fixated the same target at different gaze angles, both dorsally (lateral intraparietal cortex, LIP) and ventrally (anterior inferotemporal cortex, AIT). While eye-position modulations occurred in both areas, they were both more frequent and stronger in LIP neurons. We used an intrinsic population decoding technique, multidimensional scaling (MDS), to recover eye positions, equivalent to recovering fixated target locations. We report that eye-position based visual space in LIP was more accurate (i.e., metric). Nevertheless, the AIT spatial representation remained largely topologically correct, perhaps indicative of a categorical spatial representation (i.e., a qualitative description such as “left of” or “above” as opposed to a quantitative, metrically precise description). Additionally, we developed a simple neural model of eye position signals and illustrate that differences in single cell characteristics can influence the ability to recover target position in a population of cells. We demonstrate for the first time that the ventral stream contains sufficient information for constructing an eye-position based spatial representation. Furthermore we demonstrate, in dorsal and ventral streams as well as modeling, that target locations can be extracted directly from eye position signals in cortical visual responses without computing coordinate transforms of visual space.

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.

Shape selectivity and remapping in dorsal stream visual area LIP

We explore the visual world by making rapid eye movements (saccades) to focus on objects and locations of interest. Despite abrupt retinal image shifts, we see the world as stable. Remapping contributes to visual stability by updating the internal image with every saccade. Neurons in macaque lateral intraparietal cortex (LIP) and other brain areas update information about salient locations around the time of a saccade. The depth of information transfer remains to be thoroughly investigated. Area LIP, as part of the dorsal visual stream, is regarded as a spatially selective area, yet there is evidence that LIP neurons also encode object features. We sought to determine whether LIP remaps shape information. This knowledge is important for understanding what information is retained from each glance. We identified 82 remapping neurons. First, we presented shapes within the receptive field and tested for shape selectivity in a fixation task. Among the remapping neurons, 28 neurons (34%) were selective for shape. Second, we presented the same shapes in the future location of the receptive field around the time of the saccade and tested for shape selectivity during remapping. Thirty-one (38%) neurons were selective for shape. Of 11 neurons that were shape selective in both tasks, 5 showed significant correlation between shape selectivity in the two tasks. Across the population, there was a weak but significant correlation between responses to shape in the two tasks. Our results provide neurophysiological evidence that remapped responses in area LIP can encode shape information as well as spatial information.

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.

Neuronal responses to target onset in oculomotor and somatomotor parietal circuits differ markedly in a choice task

We often look at and sometimes reach for visible targets. Looking at a target is fast and relatively easy. By comparison, reaching for an object is slower and is associated with a larger cost. We hypothesized that, as a result of these differences, abrupt visual onsets may drive the circuits involved in saccade planning more directly and with less intermediate regulation than the circuits involved in reach planning. To test this hypothesis, we recorded discharge activity of neurons in the parietal oculomotor system (area LIP) and in the parietal somatomotor system (area PRR) while monkeys performed a visually guided movement task and a choice task. We found that in the visually guided movement task LIP neurons show a prominent transient response to target onset. PRR neurons also show a transient response, although this response is reduced in amplitude, is delayed, and has a slower rise time compared with LIP. A more striking difference is observed in the choice task. The transient response of PRR neurons is almost completely abolished and replaced with a slow buildup of activity, while the LIP response is merely delayed and reduced in amplitude. Our findings suggest that the oculomotor system is more closely and obligatorily coupled to the visual system, whereas the somatomotor system operates in a more discriminating manner.

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

Response to Comment on “In Monkeys Making Value-Based Decisions, LIP Neurons Encode Cue Salience and Not Action Value”

Newsome et al. question neither our key result, that large-penalty cues elicited stronger responses than small-penalty cues, nor our key conclusion, that neurons early in the trial signaled cue salience and not action value. Instead, they focus on subsequent neuronal activity. The patterns of delay-period activity that they note can be explained by reference to experimental methodology.

Visual Crowding at a Distance during Predictive Remapping

When we move our eyes, images of objects are displaced on the retina, yet the visual world appears stable. Oculomotor activity just prior to an eye movement contributes to perceptual stability by providing information about the predicted location of a relevant object on the retina following a saccade. It remains unclear, however, whether an object's features are represented at the remapped location. Here, we exploited the phenomenon of visual crowding to show that presaccadic remapping preserves the elementary features of objects at their predicted postsaccadic locations. Observers executed an eye movement and identified a letter probe flashed just before the saccade. Flanking stimuli were flashed around the location that would be occupied by the probe immediately following the saccade. Despite being positioned in the opposite visual field to the probe, these flankers disrupted observers' ability to identify the probe. Crucially, this "remapped crowding" interference was stronger when the flankers were visually similar to the probe than when the flanker and probe stimuli were distinct. Our findings suggest that visual processing at remapped locations is featurally dependent, providing a mechanism for achieving perceptual continuity of objects across saccades.

The lateral intraparietal area codes the location of saccade targets and not the dimension of the saccades that will be made to acquire them

Activity in the lateral intraparietal area (LIP) represents a priority map that can be used to direct attention and guide eye movements. However, it is not known whether this activity represents the location of saccade targets or the actual eye movement made to acquire them. We recorded single neurons from rhesus macaques (Macaca mulatta) while they performed memory-guided delayed saccades to characterize the response profiles of LIP cells. We then separated the saccade target from the saccade end point by saccadic adaptation, a method that induces a change in the gain of the oculomotor system. We plotted LIP activity for all three epochs of the memory-guided delayed-response task (visual, delay period, and presaccadic responses) as a function of target location and saccade end point. We found that under saccadic adaptation the response profile for all three epochs was unchanged as a function of target location. We conclude that neurons in LIP reliably represent the locations of saccade targets, not the amplitude of the saccade required to acquire those targets. Although LIP transmits target information to the motor system, that information represents the location of the target and not the amplitude of the saccade that the monkey will make.

Signal Multiplexing and Single-Neuron Computations in Lateral Intraparietal Area During Decision-Making

Previous work has revealed a remarkably direct neural correlate of decisions in the lateral intraparietal area (LIP). Specifically, firing rate has been observed to ramp up or down in a manner resembling the accumulation of evidence for a perceptual decision reported by making a saccade into (or away from) the neuron's response field (RF). However, this link between LIP response and decision formation emerged from studies where a saccadic target was always stimulating the RF during decisions, and where the neural correlate was the averaged activity of a restricted sample of neurons. Because LIP cells are (1) highly responsive to the presence of a visual stimulus in the RF, (2) heterogeneous, and (3) not clearly anatomically segregated from large numbers of neurons that fail selection criteria, the underlying neuronal computations are potentially obscured. To address this, we recorded single neuron spiking activity in LIP during a well-studied moving-dot direction-discrimination task and manipulated whether a saccade target was present in the RF during decision-making. We also recorded from a broad sample of LIP neurons, including ones conventionally excluded in prior studies. Our results show that cells multiplex decision signals with decision-irrelevant visual signals. We also observed disparate, repeating response "motifs" across neurons that, when averaged together, resemble traditional ramping decision signals. In sum, neural responses in LIP simultaneously carry decision signals and decision-irrelevant sensory signals while exhibiting diverse dynamics that reveal a broader range of neural computations than previously entertained.

Parietal Cortical Neuronal Activity Is Selective for Express Saccades

Saccadic eye movements are central to primate behavior and serve to move the eyes to visual objects of interest. Express saccades, unlike regular saccades, occur with very short reaction times, a behavior necessary for speeded reactions in goal-directed behavior. Previous studies have shown that introduction of a blank interval (gap) between the fixation point offset and the saccadic target onset leads to an increase in the number of express saccades and that the superior colliculus plays a crucial role in the generation of express saccades. A longstanding hypothesis asserted that express saccades are mediated largely by a subcortical circuit, circumventing extrastriate visual cortex. An alternative "posterior pathway" hypothesis proposed the involvement of posterior parietal cortex. In the present study, using a gap saccade task, we investigated the role of nonhuman primate's lateral intraparietal cortex (LIP) in generation of express saccades. We show that roughly half of recorded LIP neurons were modulated during the gap interval. Moreover, a group of neurons with persistent activity in a memory-guided saccade task enhanced their activity during express saccades relative to that during regular saccades. After reducing the target's certainty by increasing the potential target locations, neuronal activity remained in the similar level during express saccades but markedly reduced during regular saccades that correlated with the increase of saccadic reaction time in the regular saccade. Our results suggest that area LIP is directly involved in generating saccades in express mode.

A Scalar Neural Code for Categories in Parietal Cortex: Representing Cognitive Variables as “More” or “Less”

In this issue, Fitzgerald et al. (2013) show that LIP neurons in monkeys encode categorically distinct task conditions using a scalar code. Activity scales up or down to encode different categories, with neurons maintaining proportional levels of activity in relation to one another.