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.     

A Sensorimotor Model for Computing Intended Reach Trajectories

The presumed role of the primate sensorimotor system is to transform reach targets from retinotopic to joint coordinates for producing motor output. However, the interpretation of neurophysiological data within this framework is ambiguous, and has led to the view that the underlying neural computation may lack a well-defined structure. Here, I consider a model of sensorimotor computation in which temporal as well as spatial transformations generate representations of desired limb trajectories, in visual coordinates. This computation is suggested by behavioral experiments, and its modular implementation makes predictions that are consistent with those observed in monkey posterior parietal cortex (PPC). In particular, the model provides a simple explanation for why PPC encodes reach targets in reference frames intermediate between the eye and hand, and further explains why these reference frames shift during movement. Representations in PPC are thus consistent with the orderly processing of information, provided we adopt the view that sensorimotor computation manipulates desired movement trajectories, and not desired movement endpoints.     

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.     

Where the eye looks, the hand follows; limb-dependent magnetic misreaching in optic ataxia

The posterior parietal cortex (PPC) is thought to play an important role in the sensorimotor transformations associated with reaching movements. In humans, damage to the PPC, particularly bilateral lesions, leads to impairments of visually guided reaching movements (optic ataxia). Recent accounts of optic ataxia based upon electrophysiological recordings in monkeys have proposed that this disorder arises because of a breakdown in the tuning fields of parietal neurons responsible for integrating spatially congruent retinal, eye, and hand position signals to produce coordinated eye and hand movements . We present neurological evidence that forces a reconceptualization of this view. We report a detailed case study of a patient with a limb-dependent form of optic ataxia who can accurately reach with either hand to objects that he can foveate (thereby demonstrating coordinated eye-hand movements) but who cannot effectively decouple reach direction from gaze direction for movements executed using his right arm. The demonstration that our patient's misreaching is confined to movements executed using his right limb, and only for movements that are directed to nonfoveal targets, rules out explanations based upon simple perceptual or motor deficits but indicates an impairment in the ability to dissociate the eye and limb visuomotor systems when appropriate.     

Functional split between parietal and entorhinal cortices in the rat

Posterior parietal cortex (PPC) and medial entorhinal cortex (MEC) are important elements of the neural circuit for space, but whether representations in these areas are controlled by the same factors is unknown. We recorded single units simultaneously in PPC and MEC of freely foraging rats and found that a subset of PPC cells are tuned to specific modes of movement irrespective of the animals' location or heading, whereas grid cells in MEC expressed static spatial maps. The behavioral correlates of PPC cells switched completely when the same animals ran in a spatially structured maze or when they ran similar stereotypic sequences in an open arena. Representations in PPC were similar in identical mazes in different rooms where grid cells completely realigned their firing fields. The data suggest that representations in PPC are determined by the organization of actions while cells in MEC are driven by spatial inputs.     

The Importance of Lateral Connections in the Parietal Cortex for Generating Motor Plans

Substantial evidence has highlighted the significant role of associative brain areas, such as the posterior parietal cortex (PPC) in transforming multimodal sensory information into motor plans. However, little is known about how different sensory information, which can have different delays or be absent, combines to produce a motor plan, such as executing a reaching movement. To address these issues, we constructed four biologically plausible network architectures to simulate PPC: 1) feedforward from sensory input to the PPC to a motor output area, 2) feedforward with the addition of an efference copy from the motor area, 3) feedforward with the addition of lateral or recurrent connectivity across PPC neurons, and 4) feedforward plus efference copy, and lateral connections. Using an evolutionary strategy, the connectivity of these network architectures was evolved to execute visually guided movements, where the target stimulus provided visual input for the entirety of each trial. The models were then tested on a memory guided motor task, where the visual target disappeared after a short duration. Sensory input to the neural networks had sensory delays consistent with results from monkey studies. We found that lateral connections within the PPC resulted in smoother movements and were necessary for accurate movements in the absence of visual input. The addition of lateral connections resulted in velocity profiles consistent with those observed in human and non-human primate visually guided studies of reaching, and allowed for smooth, rapid, and accurate movements under all conditions. In contrast, Feedforward or Feedback architectures were insufficient to overcome these challenges. Our results suggest that intrinsic lateral connections are critical for executing accurate, smooth motor plans.     

Integration of Sensory and Reward Information during Perceptual Decision-Making in Lateral Intraparietal Cortex (LIP) of the Macaque Monkey

Single neurons in cortical area LIP are known to carry information relevant to both sensory and value-based decisions that are reported by eye movements. It is not known, however, how sensory and value information are combined in LIP when individual decisions must be based on a combination of these variables. To investigate this issue, we conducted behavioral and electrophysiological experiments in rhesus monkeys during performance of a two-alternative, forced-choice discrimination of motion direction (sensory component). Monkeys reported each decision by making an eye movement to one of two visual targets associated with the two possible directions of motion. We introduced choice biases to the monkeys'' decision process (value component) by randomly interleaving balanced reward conditions (equal reward value for the two choices) with unbalanced conditions (one alternative worth twice as much as the other). The monkeys'' behavior, as well as that of most LIP neurons, reflected the influence of all relevant variables: the strength of the sensory information, the value of the target in the neuron''s response field, and the value of the target outside the response field. Overall, detailed analysis and computer simulation reveal that our data are consistent with a two-stage drift diffusion model proposed by Diederich and Bussmeyer [1] for the effect of payoffs in the context of sensory discrimination tasks. Initial processing of payoff information strongly influences the starting point for the accumulation of sensory evidence, while exerting little if any effect on the rate of accumulation of sensory evidence.     

Reaches to sounds encoded in an eye-centered reference frame

A recent hypothesis suggests that neurons in the lateral intraparietal area (LIP) and the parietal reach region (PRR) encode movement plans in a common eye-centered reference frame. To test this hypothesis further, we examined how PRR neurons encode reach plans to auditory stimuli. We found that PRR activity was affected by eye and initial hand position. Population analyses, however, indicated that PRR neurons were affected more strongly by eye position than by initial hand position. These eye position effects were appropriate to maintain coding in eye coordinates. Indeed, a significant population of PRR neurons encoded reaches to auditory stimuli in an eye-centered reference frame. These results extend the hypothesis that, regardless of the modality of the sensory input or the eventual action, PRR and LIP neurons represent movement plans in a common, eye-centered representation.     

The Role of the Caudal Superior Parietal Lobule in Updating Hand Location in Peripheral Vision: Further Evidence from Optic Ataxia

Patients with optic ataxia (OA), who are missing the caudal portion of their superior parietal lobule (SPL), have difficulty performing visually-guided reaches towards extra-foveal targets. Such gaze and hand decoupling also occurs in commonly performed non-standard visuomotor transformations such as the use of a computer mouse. In this study, we test two unilateral OA patients in conditions of 1) a change in the physical location of the visual stimulus relative to the plane of the limb movement, 2) a cue that signals a required limb movement 180° opposite to the cued visual target location, or 3) both of these situations combined. In these non-standard visuomotor transformations, the OA deficit is not observed as the well-documented field-dependent misreach. Instead, OA patients make additional eye movements to update hand and goal location during motor execution in order to complete these slow movements. Overall, the OA patients struggled when having to guide centrifugal movements in peripheral vision, even when they were instructed from visual stimuli that could be foveated. We propose that an intact caudal SPL is crucial for any visuomotor control that involves updating ongoing hand location in space without foveating it, i.e. from peripheral vision, proprioceptive or predictive information.     

Choosing goals, not rules: deciding among rule-based action plans

In natural situations, movements are often directed toward locations different from that of the evoking sensory stimulus. Movement goals must then be inferred from the sensory cue based on rules. When there is uncertainty about the rule that applies for a given cue, planning a movement involves both choosing the relevant rule and computing the movement goal based on that rule. Under these conditions, it is not clear whether primates compute multiple movement goals based on all possible rules before choosing an action, or whether they first choose a rule and then only represent the movement goal associated with that rule. Supporting the former hypothesis, we show that neurons in the frontoparietal reach areas of monkeys simultaneously represent two different rule-based movement goals, which are biased by the monkeys' choice preferences. Apparently, primates choose between multiple behavioral options by weighing against each other the movement goals associated with each option.     

Representation of time by neurons in the posterior parietal cortex of the macaque

The neural basis of time perception is unknown. Here we show that neurons in the posterior parietal cortex (area LIP) represent elapsed time relative to a remembered duration. We trained rhesus monkeys to report whether the duration of a test light was longer or shorter than a remembered "standard" (316 or 800 ms) by making an eye movement to one of two choice targets. While timing the test light, the responses of LIP neurons signaled changes in the monkey's perception of elapsed time. The variability of the neural responses explained the monkey's uncertainty about its temporal judgments. Thus, in addition to their role in spatial processing and sensorimotor integration, posterior parietal neurons encode signals related to the perception of time.     

Feature-based attention in the frontal eye field and area V4 during visual search

When we search for a target in a crowded visual scene, we often use the distinguishing features of the target, such as color or shape, to guide our attention and eye movements. To investigate the neural mechanisms of feature-based attention, we simultaneously recorded neural responses in the frontal eye field (FEF) and area V4 while monkeys performed a visual search task. The responses of cells in both areas were modulated by feature attention, independent of spatial attention, and the magnitude of response enhancement was inversely correlated with the number of saccades needed to find the target. However, an analysis of the latency of sensory and attentional influences on responses suggested that V4 provides bottom-up sensory information about stimulus features, whereas the FEF provides a top-down attentional bias toward target features that modulates sensory processing in V4 and that could be used to guide the eyes to a searched-for target.     

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.     

Olfactory predictive codes and stimulus templates in piriform cortex

Neuroscientific models of sensory perception suggest that the brain utilizes predictive codes in advance of a stimulus encounter, enabling organisms to infer forthcoming sensory events. However, it is poorly understood how such mechanisms are implemented in the olfactory system. Combining high-resolution functional magnetic resonance imaging with multivariate (pattern-based) analyses, we examined the spatiotemporal evolution of odor perception in the human brain during an olfactory search task. Ensemble activity patterns in anterior piriform cortex (APC) and orbitofrontal cortex (OFC) reflected the attended odor target both before and after stimulus onset. In contrast, prestimulus ensemble representations of the odor target in posterior piriform cortex (PPC) gave way to poststimulus representations of the odor itself. Critically, the robustness of target-related patterns in PPC predicted subsequent behavioral performance. Our findings directly show that the brain generates predictive templates or "search images" in PPC, with physical correspondence to odor-specific pattern representations, to augment olfactory perception.     

Neural correlates of knowledge: stable representation of stimulus associations across variations in behavioral performance

Behavioral responses to a sensory stimulus are often guided by associative memories. These associations remain intact even when other factors determine behavior. The substrates of associative memory should therefore be identifiable by neuronal responses that are independent of behavioral choices. We tested this hypothesis using a paired-associates task in which monkeys learned arbitrary associations between pairs of visual stimuli. We examined the activity of neurons in inferior temporal cortex as the animals prepared to choose a remembered stimulus from a visual display. The activity of some neurons (22%) depended on the monkey's behavioral choice; but for a novel class of neurons (54%), activity reflected the stimulus that the monkey was instructed to choose, regardless of the behavioral response. These neurons appear to represent memorized stimulus associations that are stable across variations in behavioral performance. In addition, many neurons (74%) were modulated by the spatial arrangement of the stimuli in the display.     

Manipulating intent: evidence for a causal role of the superior colliculus in target selection

The superior colliculus (SC) is well known for its role in the motor control of saccades. Recent work has shown that it also plays a role in the selection of saccades, but a causal role in the process of target selection has not been demonstrated. We applied subthreshold microstimulation to the SC while monkeys performed a task requiring them to select a stimulus as the target for a pursuit or saccade movement. Stimulation increased the proportion of selections toward the stimulus that appeared contralateral to the site of stimulation and also decreased their latencies. For pursuit, this stimulation-induced contralateral response bias was with respect to the initial target location and not the direction of eye movement, demonstrating a causal effect on target choice distinct from any effect on motor preparation. These results show that the SC helps decide the object of the next movement, beyond its traditional responsibility of saccade production.     

State-Dependent Changes in Auditory Sensory Gating in Different Cortical Areas in Rats

Sensory gating is a process in which the brain’s response to a repetitive stimulus is attenuated; it is thought to contribute to information processing by enabling organisms to filter extraneous sensory inputs from the environment. To date, sensory gating has typically been used to determine whether brain function is impaired, such as in individuals with schizophrenia or addiction. In healthy subjects, sensory gating is sensitive to a subject’s behavioral state, such as acute stress and attention. The cortical response to sensory stimulation significantly decreases during sleep; however, information processing continues throughout sleep, and an auditory evoked potential (AEP) can be elicited by sound. It is not known whether sensory gating changes during sleep. Sleep is a non-uniform process in the whole brain with regional differences in neural activities. Thus, another question arises concerning whether sensory gating changes are uniform in different brain areas from waking to sleep. To address these questions, we used the sound stimuli of a Conditioning-testing paradigm to examine sensory gating during waking, rapid eye movement (REM) sleep and Non-REM (NREM) sleep in different cortical areas in rats. We demonstrated the following: 1. Auditory sensory gating was affected by vigilant states in the frontal and parietal areas but not in the occipital areas. 2. Auditory sensory gating decreased in NREM sleep but not REM sleep from waking in the frontal and parietal areas. 3. The decreased sensory gating in the frontal and parietal areas during NREM sleep was the result of a significant increase in the test sound amplitude.     

Optimal response of eye and hand motor systems in pointing at a visual target

In a task requiring an optimal hand pointing (with regards to both time and accuracy) at a peripheral target, there is first a saccade of the eye within 250 ms, followed 100 ms later by the hand movement. However the latency of the hand movement is poorly correlated with that of the eye movement. When the peripheral target is cut off at the onset of the saccade, there is no correlation between the error of the gaze position and the error of the hand pointing. This suggests an early parallel processing of the two motor outputs. The duration of hand movement does not change significantly when subjects either see or not see their hand (closed or open loop). In the open loop situation, the undershoot of the hand pointing increases with target eccentricity, whatever the subjects are allowed or not to do a saccade toward the target. It suggests that the encoding of eye position by itself is a poor index for an accurately guided movement of the hand.     

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.     

A deficit in covert attention after parietal cortex inactivation in the monkey

Although the parietal cortex has been repeatedly implicated in controlling attention, the nature and importance of this contribution remain unclear. Here we show that inactivating the lateral intraparietal area in monkeys delays the detection of a visual target located in the contralateral visual field. This effect was observed using different visual scene configurations, e.g., with distractors that differ in number or that differ from the target by a conjunction of shape and color or by a single feature. Since eye movements were not allowed during the searching tasks, these results argue for an unambiguous role of the parietal cortex in the top-down control of attentional deployment in space.