Single neurons in posterior parietal cortex of monkeys encode cognitive set

The primate posterior parietal cortex (PPC), part of the dorsal visual pathway, is best known for its role in encoding salient spatial information. Yet there are indications that neural activity in the PPC can also be modulated by nonspatial task-related information. In this study, we tested whether neurons in the PPC encode signals related to cognitive set, that is, the preparation to perform a particular task. Cognitive set has previously been associated with the frontal cortex but not the PPC. In this study, monkeys performed a cognitive set shifting paradigm in which they were cued in advance to apply one of two different task rules to the subsequent stimulus on every trial. Here we show that a subset of neurons in the PPC, concentrated in the lateral bank of the intraparietal sulcus and on the angular gyrus, responds selectively to cues for different task rules.     

Spatio-temporal updating in the left posterior parietal cortex

Adopting an unusual posture can sometimes give rise to paradoxical experiences. For example, the subjective ordering of successive unseen tactile stimuli delivered to the two arms can be affected when people cross them. A growing body of evidence now highlights the role played by the parietal cortex in spatio-temporal information processing when sensory stimuli are delivered to the body or when actions are executed; however, little is known about the neural basis of such paradoxical feelings resulting from such unusual limb positions. Here, we demonstrate increased fMRI activation in the left posterior parietal cortex when human participants adopted a crossed hands posture with their eyes closed. Furthermore, by assessing tactile temporal order judgments (TOJs) in the same individuals, we observed a positive association between activity in this area and the degree of reversal in TOJs resulting from crossing arms. The strongest positive association was observed in the left intraparietal sulcus. This result implies that the left posterior parietal cortex may be critically involved in monitoring limb position and in spatio-temporal binding when serial events are delivered to the limbs.     

Tracking route progression in the posterior parietal cortex

Quick and efficient traversal of learned routes is critical to the survival of many animals. Routes can be defined by both the ordering of navigational epochs, such as continued forward motion or execution of a turn, and the distances separating them. The neural substrates conferring the ability to fluidly traverse complex routes are not well understood, but likely entail interactions between frontal, parietal, and rhinal cortices and the hippocampus. This paper demonstrates that posterior parietal cortical neurons map both individual and multiple navigational epochs with respect to their order in a route. In direct contrast to spatial firing patterns of hippocampal neurons, parietal neurons discharged in a place- and direction-independent fashion. Parietal route maps were scalable and versatile in that they were independent of the size and spatial configuration of navigational epochs. The results provide a framework in which to consider parietal function in spatial cognition.     

Neural correlates of social target value in macaque parietal cortex

Animals as diverse as arthropods [1], fish [2], reptiles [3], birds [4], and mammals, including primates [5], depend on visually acquired information about conspecifics for survival and reproduction. For example, mate localization often relies on vision [6], and visual cues frequently advertise sexual receptivity or phenotypic quality [5]. Moreover, recognizing previously encountered competitors or individuals with preestablished territories [7] or dominance status [1, 5] can eliminate the need for confrontation and the associated energetic expense and risk for injury. Furthermore, primates, including humans, tend to look toward conspecifics and objects of their attention [8, 9], and male monkeys will forego juice rewards to view images of high-ranking males and female genitalia [10]. Despite these observations, we know little about how the brain evaluates social information or uses this appraisal to guide behavior. Here, we show that neurons in the primate lateral intraparietal area (LIP), a cortical area previously linked to attention and saccade planning [11, 12], signal the value of social information when this assessment influences orienting decisions. In contrast, social expectations had no impact on LIP neuron activity when monkeys were not required to make a choice. These results demonstrate for the first time that parietal cortex carries abstract, modality-independent target value signals that inform the choice of where to look.     

Sensory and behavioral properties of neurons in posterior parietal cortex of the awake, trained monkey.

Neurons in posterior parietal cortex of the awake, trained monkey respond to passive visual and/or somatosensory stimuli. In general, the receptive fields of these cells are large and nonspecific. When these neurons are studied during visually guided hand movements and eye movements, most of their activity can be accounted for by passive sensory stimulation. However, for some visual cells, the response to a stimulus is enhanced when it is to be the target for a saccadic eye movement. This enhancement is selective for eye movements into the visual receptive field since it does not occur with eye movements to other parts of the visual field. Cells that discharge in association with a visual fixation task have foveal receptive fields and respond to the spots of light used as fixation targets. Cells discharging selectively in association with different directions of tracking eye movements have directionally selective responses to moving visual stimuli. Every cell in our sample discharging in association with movement could be driven by passive sensory stimuli. We conclude that the activity of neurons in posterior parietal cortex is dependent on and indicative of external stimuli but not predictive of movement.     

Representation of color stimuli in awake macaque primary visual cortex

We investigated the responses of single neurons in primary visual cortex (area V1) of awake monkeys to chromatic stimuli. Chromatic tuning properties, determined for homogeneous color patches presented on a neutral gray background, varied strongly between cells. The continuum of preferred chromaticities and tuning widths indicated a distributed representation of color signals in V1. When stimuli were presented on colored backgrounds, chromatic tuning was different in most neurons, and the changes in tuning were consistent with some degree of sensitivity of the neurons to the chromatic contrast between stimulus and background. Quantitatively, the average response changes matched the magnitudes of color induction effects measured in human subjects under corresponding stimulus conditions.     

Representation of others' action by neurons in monkey medial frontal cortex

Successful social interaction depends on not only the ability to identify with others but also the ability to distinguish between aspects of self and others. Although there is considerable knowledge of a shared neural substrate between self-action and others' action, it remains unknown where and how in the brain the action of others is uniquely represented. Exploring such agent-specific neural codes is important because one's action and intention can differ between individuals. Moreover, the assignment of social agency breaks down in a range of mental disorders. Here, using two monkeys monitoring each other's action for adaptive behavioral planning, we show that the medial frontal cortex (MFC) contains a group of neurons that selectively encode others' action. These neurons, observed in both dominant and submissive monkeys, were significantly more prevalent in the dorsomedial convexity region of the MFC including the pre-supplementary motor area than in the cingulate sulcus region of the MFC including the rostral cingulate motor area. Further tests revealed that the difference in neuronal activity was not due to gaze direction or muscular activity. We suggest that the MFC is involved in self-other differentiation in the domain of motor action and provides a fundamental neural signal for social learning.     

Characterization of visual percepts evoked by noninvasive stimulation of the human posterior parietal cortex

Phosphenes are commonly evoked by transcranial magnetic stimulation (TMS) to study the functional organization, connectivity, and excitability of the human visual brain. For years, phosphenes have been documented only from stimulating early visual areas (V1-V3) and a handful of specialized visual regions (V4, V5/MT+) in occipital cortex. Recently, phosphenes were reported after applying TMS to a region of posterior parietal cortex involved in the top-down modulation of visuo-spatial processing. In the present study, we systematically characterized parietal phosphenes to determine if they are generated directly by local mechanisms or emerge through indirect activation of other visual areas. Using technology developed in-house to record the subjective features of phosphenes, we found no systematic differences in the size, shape, location, or frame-of-reference of parietal phosphenes when compared to their occipital counterparts. In a second experiment, discrete deactivation by 1 Hz repetitive TMS yielded a double dissociation: phosphene thresholds increased at the deactivated site without producing a corresponding change at the non-deactivated location. Overall, the commonalities of parietal and occipital phosphenes, and our ability to independently modulate their excitability thresholds, lead us to conclude that they share a common neural basis that is separate from either of the stimulated regions.     

Proprioceptive alignment of visual and somatosensory maps in the posterior parietal cortex

A touch on one hand can enhance the response to a visual stimulus delivered at a nearby location [1, 2], improving our interactions with the external world. In order to keep such visual-tactile spatial interactions effective, the brain updates the continuous postural changes, like those typically accompanying hand actions, through proprioception, thus maintaining the somatosensory and visual maps in spatial register [2, 3]. The posterior parietal cortex (PPC) might be critical for such a spatial remapping [4]; nevertheless, a direct causal demonstration of its involvement is lacking. Here, we found that unattended touches to one hand enhanced visual sensitivity for phosphenes induced by occipital trancranial magnetic stimulation (TMS) [5] when the touched hand was spatially coincident to the reported location of the phosphenes in external space. Notably, this spatially specific crossmodal facilitation was maintained after hand crossing, suggesting an efficient visual-tactile remapping. Critically, after 1 Hz repetitive TMS interference [6] over the PPC, but not over the primary somatosensory cortex, phosphene detection was still enhanced by spatially coincident touches with uncrossed hands, but it was enhanced by spatially noncoincident touches after hand crossing. This is the first causal evidence in humans that the PPC constantly updates the representation of the body in space in order to facilitate crossmodal interactions.     

Fix your eyes in the space you could reach: neurons in the macaque medial parietal cortex prefer gaze positions in peripersonal space

Interacting in the peripersonal space requires coordinated arm and eye movements to visual targets in depth. In primates, the medial posterior parietal cortex (PPC) represents a crucial node in the process of visual-to-motor signal transformations. The medial PPC area V6A is a key region engaged in the control of these processes because it jointly processes visual information, eye position and arm movement related signals. However, to date, there is no evidence in the medial PPC of spatial encoding in three dimensions. Here, using single neuron recordings in behaving macaques, we studied the neural signals related to binocular eye position in a task that required the monkeys to perform saccades and fixate targets at different locations in peripersonal and extrapersonal space. A significant proportion of neurons were modulated by both gaze direction and depth, i.e., by the location of the foveated target in 3D space. The population activity of these neurons displayed a strong preference for peripersonal space in a time interval around the saccade that preceded fixation and during fixation as well. This preference for targets within reaching distance during both target capturing and fixation suggests that binocular eye position signals are implemented functionally in V6A to support its role in reaching and grasping.     

Dynamic social adaptation of motion-related neurons in primate parietal cortex

Social brain function, which allows us to adapt our behavior to social context, is poorly understood at the single-cell level due largely to technical limitations. But the questions involved are vital: How do neurons recognize and modulate their activity in response to social context? To probe the mechanisms involved, we developed a novel recording technique, called multi-dimensional recording, and applied it simultaneously in the left parietal cortices of two monkeys while they shared a common social space. When the monkeys sat near each other but did not interact, each monkey's parietal activity showed robust response preference to action by his own right arm and almost no response to action by the other's arm. But the preference was broken if social conflict emerged between the monkeys-specifically, if both were able to reach for the same food item placed on the table between them. Under these circumstances, parietal neurons started to show complex combinatorial responses to motion of self and other. Parietal cortex adapted its response properties in the social context by discarding and recruiting different neural populations. Our results suggest that parietal neurons can recognize social events in the environment linked with current social context and form part of a larger social brain network.     

Multimodal integration for the representation of space in the posterior parietal cortex.

The posterior parietal cortex has long been considered an ''association'' area that combines information from different sensory modalities to form a cognitive representation of space. However, until recently little has been known about the neural mechanisms responsible for this important cognitive process. Recent experiments from the author''s laboratory indicate that visual, somatosensory, auditory and vestibular signals are combined in areas LIP and 7a of the posterior parietal cortex. The integration of these signals can represent the locations of stimuli with respect to the observer and within the environment. Area MSTd combines visual motion signals, similar to those generated during an observer''s movement through the environment, with eye-movement and vestibular signals. This integration appears to play a role in specifying the path on which the observer is moving. All three cortical areas combine different modalities into common spatial frames by using a gain-field mechanism. The spatial representations in areas LIP and 7a appear to be important for specifying the locations of targets for actions such as eye movements or reaching; the spatial representation within area MSTd appears to be important for navigation and the perceptual stability of motion signals.     

A common reference frame for movement plans in the posterior parietal cortex

Orchestrating a movement towards a sensory target requires many computational processes, including a transformation between reference frames. This transformation is important because the reference frames in which sensory stimuli are encoded often differ from those of motor effectors. The posterior parietal cortex has an important role in these transformations. Recent work indicates that a significant proportion of parietal neurons in two cortical areas transforms the sensory signals that are used to guide movements into a common reference frame. This common reference frame is an eye-centred representation that is modulated by eye-, head-, body- or limb-position signals. A common reference frame might facilitate communication between different areas that are involved in coordinating the movements of different effectors. It might also be an efficient way to represent the locations of different sensory targets in the world.     

Cortical local field potential encodes movement intentions in the posterior parietal cortex

The cortical local field potential (LFP) is a summation signal of excitatory and inhibitory dendritic potentials that has recently become of increasing interest. We report that LFP signals in the parietal reach region (PRR) of the posterior parietal cortex of macaque monkeys have temporal structure that varies with the type of planned or executed motor behavior. LFP signals from PRR provide better decode performance for reaches compared to saccades and have stronger coherency with simultaneously recorded spiking activity during the planning of reach movements than during saccade planning. LFP signals predict the animal's behavioral state (e.g., planning a reach or saccade) and the direction of the currently planned movement from single-trial information. This new evidence provides further support for a role of the parietal cortex in movement planning and the potential application of LFP signals for a brain-machine interface.     

Posterior parietal cortex neurons encode target motion in world-centered coordinates

The motion areas of posterior parietal cortex extract information on visual motion for perception as well as for the guidance of movement. It is usually assumed that neurons in posterior parietal cortex represent visual motion relative to the retina. Current models describing action guided by moving objects work successfully based on this assumption. However, here we show that the pursuit-related responses of a distinct group of neurons in area MST of monkeys are at odds with this view. Rather than signaling object image motion on the retina, they represent object motion in world-centered coordinates. This representation may simplify the coordination of object-directed action and ego motion-invariant visual perception.     

fMRI adaptation reveals mirror neurons in human inferior parietal cortex

Mirror neurons, as originally described in the macaque, have two defining properties [1, 2]: They respond specifically to a particular action (e.g., bringing an object to the mouth), and they produce their action-specific responses independent of whether the monkey executes the action or passively observes a conspecific performing the same action. In humans, action observation and action execution engage a network of frontal, parietal, and temporal areas. However, it is unclear whether these responses reflect the activity of a single population that represents both observed and executed actions in a common neural code or the activity of distinct but overlapping populations of exclusively perceptual and motor neurons [3]. Here, we used fMRI adaptation to show that the right inferior parietal lobe (IPL) responds independently to specific actions regardless of whether they are observed or executed. Specifically, responses in the right IPL were attenuated when participants observed a recently executed action relative to one that had not previously been performed. This adaptation across action and perception demonstrates that the right IPL responds selectively to the motoric and perceptual representations of actions and is the first evidence for a neural response in humans that shows both defining properties of mirror neurons.     

The role of the posterior parietal cortex in coordinate transformations for visual-motor integration

Lesion to the posterior parietal cortex in monkeys and humans produces spatial deficits in movement and perception. In recording experiments from area 7a, a cortical subdivision in the posterior parietal cortex in monkeys, we have found neurons whose responses are a function of both the retinal location of visual stimuli and the position of the eyes in the orbits. By combining these signals area 7 a neurons code the location of visual stimuli with respect to the head. However, these cells respond over only limited ranges of eye positions (eye-position-dependent coding). To code location in craniotopic space at all eye positions (eye-position-independent coding) an additional step in neural processing is required that uses information distributed across populations of area 7a neurons. We describe here a neural network model, based on back-propagation learning, that both demonstrates how spatial location could be derived from the population response of area 7a neurons and accurately accounts for the observed response properties of these neurons.     

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.     

Craniotopic updating of visual space across saccades in the human posterior parietal cortex

The neural mechanisms underlying the craniotopic updating of visual space across saccadic eye movements are poorly understood. Previous single-unit recording studies in primates and clinical studies in brain-damaged patients have shown that the posterior parietal cortex (PPC) has a key role in this process. In the present study, we used single-pulse transcranial magnetic stimulation (TMS) to disrupt the processing within the PPC during a task that requires craniotopic updating: double saccades. In this task, two targets are presented in quick succession and the subject is required to make a saccade to each location as accurately as possible. We show here that TMS delivered to the PPC just prior to the second saccade effectively disrupts the craniotopic coding normally observed in this task. This causes subjects to revert to saccades more consistent with a representation of the targets based on their positions relative to one another. By contrast, stimulation at earlier times between the two saccades did not disrupt performance. These results suggest that extraretinal information generated during the first perisaccadic period is not put into functional use until just prior to the second saccade.     

Only coherent spiking in posterior parietal cortex coordinates looking and reaching

Here, we report that temporally patterned, coherent spiking activity in the posterior parietal cortex (PPC) coordinates the timing of looking and reaching. Using a spike-field approach, we identify a population of parietal area LIP neurons that fire spikes coherently with 15 Hz beta-frequency LFP activity. The firing rate of coherently active neurons predicts the reaction times (RTs) of coordinated reach-saccade movements but not of saccades when made alone. Area LIP neurons that do not fire coherently do not predict RT of either movement type. Similar beta-band LFP activity is present in the parietal reach region but not nearby visual area V3d. This suggests that coherent spiking activity in PPC can control reaches and saccades together. We propose that the neural mechanism of coordination involves a shared representation that acts to slow or speed movements together.