Parietal Reach Region Neurons Research Articles

Single Units in the Posterior Parietal Cortex Encode Patterns of Bimanual Coordination.

Bimanual coordination is critical for a broad array of behaviors. Drummers, for example, must carefully coordinate movements of their 2 arms, sometimes beating on the same drum and sometimes on different ones. While coordinated behavior is well-studied, the early stages of planning are not well understood. In the parietal reach region(PRR) of the posterior parietal cortex (PPC), the presence of neurons that modulate when either arm moves by itself has been taken as evidence for a role in bimanual coordination. To test this notion, we recorded neurons during both unilateral and bimanual movements. We find that the activity that precedes an ipsilateral arm movement is primarily a sensory response to a target in the neuron's visual receptive field and not a plan to move the ipsilateral arm. In contrast, the activity that precedes a contralateral arm movement is the sum of a movement plan plus a sensory response. Despite not coding ipsilateral arm movements, about half of neurons discriminate between different patterns of bimanual movements. These results provide direct evidence that PRR neurons represent bimanual reach plans, and suggest that bimanual coordination originates in the sensory-to-motor processing stream prior to the motor cortex, within the PPC.

The parietal reach region selectively anti-synchronizes with dorsal premotor cortex during planning.

Recent reports have indicated that oscillations shared across distant cortical regions can enhance their connectivity, but do coherent oscillations ever diminish connectivity? We investigated oscillatory activity in two distinct reach-related regions in the awake behaving monkey (Macaca mulatta): the parietal reach region (PRR) and the dorsal premotor cortex (PMd). PRR and PMd were found to oscillate at similar frequencies (beta, 15-30 Hz) during periods of fixation and movement planning. At first glance, the stronger oscillator of the two, PRR, would seem to drive the weaker, PMd. However, a more fine-grained measure, the partial spike-field coherence, revealed a different relationship. Relative to global beta-band activity in the brain, action potentials in PRR anti-synchronize with PMd oscillations. These data suggest that, rather than driving PMd during planning, PRR neurons fire in such a way that they are less likely to communicate information to PMd.

The parietal reach region is limb specific and not involved in eye-hand coordination

Primates frequently reach toward visual targets. Neurons in early visual areas respond to stimuli in the contralateral visual hemifield and without regard to which limb will be used to reach toward that target. In contrast, neurons in motor areas typically respond when reaches are performed using the contralateral limb and with minimal regard to the visuospatial location of the target. The parietal reach region (PRR) is located early in the visuomotor processing hierarchy. PRR neurons are significantly modulated when targets for either limb or eye movement appear, similar to early sensory areas; however, they respond to targets in either visual field, similar to motor areas. The activity could reflect the subject's attentional locus, movement of a specific effector, or a related function, such as coordinating eye-arm movements. To examine the role of PRR in the visuomotor pathway, we reversibly inactivated PRR. Inactivation effects were specific to contralateral limb movements, leaving ipsilateral limb and saccadic movements intact. Neither visual hemifield bias nor visual attention deficits were observed. Thus our results are consistent with a motoric rather than visual organization in PRR, despite its early location in the visuomotor pathway. We found no effects on the temporal coupling of coordinated saccades and reaches, suggesting that this mechanism lies downstream of PRR. In sum, this study clarifies the role of PRR in the visuomotor hierarchy: despite its early position, it is a limb-specific area influencing reach planning and is positioned upstream from an active eye-hand coordination-coupling mechanism.

Volitional Control of Neural Activity Relies on the Natural Motor Repertoire

The results from recent brain-machine interface (BMI) studies suggest that it may be more efficient to use simple arbitrary relationships between individual neuron activity and BMI movements than the complex relationship observed between neuron activity and natural movements. This idea is based on the assumption that individual neurons can be conditioned independently regardless of their natural movement association. We tested this assumption in the parietal reach region (PRR), an important candidate area for BMIs in which neurons encode the target location for reaching movements. Monkeys could learn to elicit arbitrarily assigned activity patterns, but the seemingly arbitrary patterns always belonged to the response set for natural reaching movements. Moreover, neurons that are free from conditioning showed correlated responses with the conditioned neurons as if they encoded common reach targets. Thus, learning was accomplished by finding reach targets (intrinsic variable of PRR neurons) for which the natural response of reach planning could approximate the arbitrary patterns. Our results suggest that animals learn to volitionally control single-neuron activity in PRR by preferentially exploring and exploiting their natural movement repertoire. Thus, for optimal performance, BMIs utilizing neural signals in PRR should harness, not disregard, the activity patterns in the natural sensorimotor repertoire.

Inactivation of the Parietal Reach Region Causes Optic Ataxia, Impairing Reaches but Not Saccades

Lesions in human posterior parietal cortex can cause optic ataxia (OA), in which reaches but not saccades to visual objects are impaired, suggesting separate visuomotor pathways for the two effectors. In monkeys, one potentially crucial area for reach control is the parietal reach region (PRR), in which neurons respond preferentially during reach planning as compared to saccade planning. However, direct causal evidence linking the monkey PRR to the deficits observed in OA is missing. We thus inactivated part of the macaque PRR, in the medial wall of the intraparietal sulcus, and produced the hallmarks of OA, misreaching for peripheral targets but unimpaired saccades. Furthermore, reach errors were larger for the targets preferred by the neural population local to the injection site. These results demonstrate that PRR is causally involved in reach-specific visuomotor pathways, and reach goal disruption in PRR can be a neural basis of OA.

A computational model of posterior parietal circuits during decision making and sequential planning

In the posterior parietal cortex (PPC), three anatomically separated but reciprocally interconnected subareas, the lateral intraparietal area (LIP), parietal reach region (PRR) and dorsal area 5 (area 5d), are involved in sensorimotor transformation during planning of eye/arm movements. We have previously designed the saccade/reach effector choice and sequential reach paradigms to dissociate cognitive and executive planning activity in PPC. During saccade/reach choice, LIP and PRR encodes potential saccade/reach plans in parallel before effector decision is formed, and the selected saccade/reach plans thereafter [1], whereas area 5d only reflects the decision outcome [2]. During sequential reach, PRR encodes both immediate and subsequent goals [3], whereas area 5d only represents the immediate upcoming reach [4]. Based on the experimental results above, we propose a network model to conceive the functional connectivity across these areas. The model is composed of an upstream layer representing the abstract motor intentions and a down-stream layer representing concrete motor commands. The up-stream layer consists of LIP and PRR neurons preferring different directions for saccade and reach, respectively, and two populations compete against each other. The down-stream layer is composed of area 5d neurons preferring arm movements to different directions. In each neuronal pool, each leaky integrate-andfire neuron excites others representing nearby targets but inhibits the remaining. The up-stream layer also feed-forwards to the down-stream layer to excite the neurons preferring the same effector and nearby target but to inhibit others. Furthermore, each LIP and PRR neuron receives self-excitation whose magnitudes are modulated by the rule-based behavioral context, reflecting the topdown feedback. Our simulation results show that, during the effector choice and instructed tasks, the effector information is ambiguous at first so that both LIP and PRR show strong responses and counterbalance the total input to area 5d. Once effector information is determined by either choice or instruction, LIP and PRR activities differentiate to trigger or suppress area 5d activity. During the classical memory saccade/reach tasks, effector information is given at the cue onset so that LIP and PRR activities began to differentiate and area 5d fires immediately. During the sequential reaching task, after two targets are simultaneously presented, the activity of the PRR encoding the 1st goal increases faster while the activity of the PRR encoding the 2nd goal increases slower but lasts longer due to the different recurrent connections modulated by the behavioral context. Consequentially, only the activity of the area 5d neuron encoding the 1st goal is elevated before the GO signal. Once the first reach is completed, the area 5d neuron preferring the 2nd goal begins to fire because top-down context information (efference copy in this case) reduces the strength of recurrent connection for the PRR neuron coding the 1st goal. Preliminary results indicate that our model captures all characteristics of neural activity we have observed so far. Our ongoing modeling work will help reveal the network mechanisms underlying the operation of the parietal sensorimotor circuits.

The representations of reach endpoints in posterior parietal cortex depend on which hand does the reaching

Neurons in the parietal reach region (PRR) have been implicated in the sensory-to-motor transformation required for reaching toward visually defined targets. The neurons in each cortical hemisphere might be specifically involved in planning movements of just one limb, or the PRR might code reach endpoints generically, independent of which limb will actually move. Previous work has shown that the preferred directions of PRR neurons are similar for right and left limb movements but that the amplitude of modulation may vary greatly. We now test the hypothesis that frames of reference and eye and hand gain field modulations will, like preferred directions, be independent of which hand moves. This was not the case. Many neurons show clear differences in both the frame of reference as well as in direction and strength of gain field modulations, depending on which hand is used to reach. The results suggest that the information that is conveyed from the PRR to areas closer to the motor output (the readout from the PRR) is different for each limb and that individual PRR neurons contribute either to controlling the contralateral-limb or else bimanual-limb control.

A Relative Position Code for Saccades in Dorsal Premotor Cortex

Spatial computations underlying the coordination of the hand and eye present formidable geometric challenges. One way for the nervous system to simplify these computations is to directly encode the relative position of the hand and the center of gaze. Neurons in the dorsal premotor cortex (PMd), which is critical for the guidance of arm-reaching movements, encode the relative position of the hand, gaze, and goal of reaching movements. This suggests that PMd can coordinate reaching movements with eye movements. Here, we examine saccade-related signals in PMd to determine whether they also point to a role for PMd in coordinating visual-motor behavior. We first compared the activity of a population of PMd neurons with a population of parietal reach region (PRR) neurons. During center-out reaching and saccade tasks, PMd neurons responded more strongly before saccades than PRR neurons, and PMd contained a larger proportion of exclusively saccade-tuned cells than PRR. During a saccade relative position-coding task, PMd neurons encoded saccade targets in a relative position code that depended on the relative position of gaze, the hand, and the goal of a saccadic eye movement. This relative position code for saccades is similar to the way that PMd neurons encode reach targets. We propose that eye movement and eye position signals in PMd do not drive eye movements, but rather provide spatial information that links the control of eye and arm movements to support coordinated visual-motor behavior.

Using a Compound Gain Field to Compute a Reach Plan

A gain field, the scaling of a tuned neuronal response by a postural signal, may help support neuronal computation. Here, we characterize eye and hand position gain fields in the parietal reach region (PRR). Eye and hand gain fields in individual PRR neurons are similar in magnitude but opposite in sign to one another. This systematic arrangement produces a compound gain field that is proportional to the distance between gaze location and initial hand position. As a result, the visual response to a target for an upcoming reach is scaled by the initial gaze-to-hand distance. Such a scaling is similar to what would be predicted in a neural network that mediates between eye- and hand-centered representations of target location. This systematic arrangement supports a role of PRR in visually guided reaching and provides strong evidence that gain fields are used for neural computations.

Parietal Reach Region Encodes Reach Depth Using Retinal Disparity and Vergence Angle Signals

Performing a visually guided reach requires the ability to perceive the egocentric distance of a target in three-dimensional space. Previous studies have shown that the parietal reach region (PRR) encodes the two-dimensional location of frontoparallel targets in an eye-centered reference frame. To investigate how a reach target is represented in three dimensions, we recorded the spiking activity of PRR neurons from two rhesus macaques trained to fixate and perform memory reaches to targets at different depths. Reach and fixation targets were configured to explore whether neural activity directly reflects egocentric distance as the amplitude of the required motor command, which is the absolute depth of the target, or rather the relative depth of the target with reference to fixation depth. We show that planning activity in PRR represents the depth of the reach target as a function of disparity and fixation depth, the spatial parameters important for encoding the depth of a reach goal in an eye centered reference frame. The strength of modulation by disparity is maintained across fixation depth. Fixation depth gain modulates disparity tuning while preserving the location of peak tuning features in PRR neurons. The results show that individual PRR neurons code depth with respect to the fixation point, that is, in eye centered coordinates. However, because the activity is gain modulated by vergence angle, the absolute depth can be decoded from the population activity.

Non-spatial, motor-specific activation in posterior parietal cortex

A localized cluster of neurons in macaque posterior parietal cortex, termed the parietal reach region (PRR), is activated when a reach is planned to a visible or remembered target. To explore the role of PRR in sensorimotor transformations, we tested whether cells would be activated when a reach is planned to an as-yet unspecified goal. Over one-third of PRR cells increased their firing after an instruction to prepare a reach, but not after an instruction to prepare a saccade, when the target of the movement remained unknown. A partially overlapping population (two-thirds of cells) was activated when the monkey was informed of the target location but not the type of movement to be made. Thus a subset of PRR neurons separately code spatial and effector-specific information, consistent with a role in specifying potential motor responses to particular targets.

Comparison of neural activity preceding reaches to auditory and visual stimuli in the parietal reach region.

We examined the responses of neurons in the parietal reach region (PRR) during reaches to the remembered locations of auditory or visual stimuli. We found that the firing rate of PRR neurons contained information about the location of auditory and visual stimuli. For neurons tested with visual stimuli, the amount of information remained constant throughout the task. In contrast, for neurons tested with auditory stimuli, the amount of target-location information increased as the trial evolved. During the reach period of the task, the amount of information that was carried by neurons tested with auditory stimuli was not statistically different from the amount carried by neurons tested with visual stimuli. We interpret these data to suggest that the type of information that PRR neurons encode evolves throughout a task.

The parietal reach region codes the next planned movement in a sequential reach task.

Distinct subregions of the posterior parietal cortex contribute to planning different movements. The parietal reach region (PRR) is active during the delay period of a memory-guided reach task but generally not active during a memory-guided saccade task. We explored whether the reach planning activity in PRR is related to remembering targets for reaches or if it is related to specifying the reach that the monkey is about to perform. Monkeys were required to remember two target locations and then reach to them in sequence. Before the movements were executed, PRR neurons predominantly represented the reach about to be performed and only rarely represented the remembered target for the second reach. This indicates the area plays a role in specifying the target for the impending reach and may not contribute to storing the memory of subsequent reach targets.

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.

Saccade-related activity in the parietal reach region.

In previous experiments, we showed that cells in the parietal reach region (PRR) in monkey posterior parietal cortex code intended reaching movements in an eye-centered frame of reference. These cells are more active when an arm compared with an eye movement is being planned. Despite this clear preference for arm movements, we now report that PRR neurons also fire around the time of a saccade. Of 206 cells tested, 29% had perisaccadic activity in a delayed-saccade task. Two findings indicate that saccade-related activity does not reflect saccade planning or execution. First, activity is often peri- or postsaccadic but seldom presaccadic. Second, cells with saccade-related activity were no more likely to show strong saccadic delay period activity than cells without saccade-related activity. These findings indicate that PRR cells do not take part in saccade planning. Instead, the saccade-related activity in PRR may reflect cross-coupling between reach and saccade pathways that may be used to facilitate eye-hand coordination. Alternatively, saccade-related activity may reflect eye position information that could be used to maintain an eye-centered representation of intended reach targets across eye movements.