Kostas Hadjidimitrakis

Eye position encoding in three-dimensional space: integration of version and vergence signals in the medial posterior parietal cortex.

Eye position signals are pivotal in the visuomotor transformations performed by the posterior parietal cortex (PPC), but to date there are few studies addressing the influence of vergence angle upon single PPC neurons. In the present study, we investigated the influence on single neurons of the medial PPC area V6A of vergence and version signals. Single-unit activity was recorded from V6A in two Macaca fascicularis fixating real targets in darkness. The fixation targets were placed at eye level and at different vergence and version angles within the peripersonal space. Few neurons were modulated by version or vergence only, while the majority of cells were affected by both signals. We advance here the hypothesis that gaze-modulated V6A cells are able to encode gazed positions in the three-dimensional space. In single cells, version and vergence influenced the discharge with variable time course. In several cases, the two gaze variables influence neural discharges during only a part of the fixation time, but, more often, their influence persisted through large parts of it. Cells discharging for the first 400–500 ms of fixation could signal the arrival of gaze (and/or of spotlight of attention) in a new position in the peripersonal space. Cells showing a more sustained activity during the fixation period could better signal the location in space of the gazed objects. Both signals are critical for the control of upcoming or ongoing arm movements, such as those needed to reach and grasp objects located in the peripersonal space.

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.

Common Neural Substrate for Processing Depth and Direction Signals for Reaching in the Monkey Medial Posterior Parietal Cortex

Many psychophysical studies suggest that target depth and direction during reaches are processed independently, but the neurophysiological support to this view is so far limited. Here, we investigated the representation of reach depth and direction by single neurons in area V6A of the medial posterior parietal cortex (PPC) of macaques, while a fixation-to-reach task in 3-dimensional (3D) space was performed. We found that, in a substantial percentage of V6A neurons, depth and direction signals jointly influenced fixation, planning, and arm movement-related activity. While target depth and direction were equally encoded during fixation, depth tuning became stronger during arm movement planning, execution, and target holding. The spatial tuning of fixation activity was often maintained across epochs, and depth tuning persisted more than directional tuning across epochs. These findings support for the first time the existence of a common neural substrate for the encoding of target depth and direction during reaches in the PPC. Present results also highlight the presence of several types of V6A cells that process independently or jointly signals about eye position and arm movement planning and execution in order to control reaches in 3D space. A conceptual framework for the processing of depth and direction for reaching is proposed.

Body-Centered, Mixed, but not Hand-Centered Coding of Visual Targets in the Medial Posterior Parietal Cortex During Reaches in 3D Space

The frames of reference used by neurons in posterior parietal cortex (PPC) to encode spatial locations during arm reaching movements is a debated topic in modern neurophysiology. Traditionally, target location, encoded in retinocentric reference frame (RF) in caudal PPC, was assumed to be serially transformed to body-centered and then hand-centered coordinates rostrally. However, recent studies suggest that these transformations occur within a single area. The caudal PPC area V6A has been shown to represent reach targets in eye-centered, body-centered, and a combination of both RFs, but the presence of hand-centered coding has not been yet investigated. To examine this issue, 141 single neurons were recorded from V6A in 2 Macaca fascicularis monkeys while they performed a foveated reaching task in darkness. The targets were presented at different distances and lateralities from the body and were reached from initial hand positions located at different depths. Most V6A cells used body-centered, or mixed body- and hand-centered coordinates. Only a few neurons used pure hand-centered coordinates, thus clearly distinguishing V6A from nearby PPC regions. Our findings support the view of a gradual RF transformation in PPC and also highlight the impact of mixed frames of reference.

Mixed Body/Hand Reference Frame for Reaching in 3D Space in Macaque Parietal Area PEc

Abstract The neural correlates of coordinate transformations from vision to action are expressed in the activity of posterior parietal cortex (PPC). It has been demonstrated that among the medial‐most areas of the PPC, reaching targets are represented mainly in hand‐centered coordinates in area PE, and in eye‐centered, body‐centered, and mixed body/hand‐centered coordinates in area V6A. Here, we assessed whether neurons of area PEc, located between V6A and PE in the medial PPC, encode targets in body‐centered, hand‐centered, or mixed frame of reference during planning and execution of reaching. We studied 104 PEc cells in 3 Macaca fascicularis. The animals performed a reaching task toward foveated targets located at different depths and directions in darkness, starting with the hand from 2 positions located at different depths, one next to the trunk and the other far from it. We show that most PEc neurons encoded targets in a mixed body/hand‐centered frame of reference. Although the effect of hand position was often rather strong, it was not as strong as reported previously in area PE. Our results suggest that area PEc represents an intermediate node in the gradual transformation from vision to action that takes place in the reaching network of the dorsomedial PPC.

Overlapping representations for reach depth and direction in caudal superior parietal lobule of macaques

Reaching movements in the real world have typically a direction and a depth component. Despite numerous behavioral studies, there is no consensus on whether reach coordinates are processed in separate or common visuomotor channels. Furthermore, the neural substrates of reach depth in parietal cortex have been ignored in most neurophysiological studies. In the medial posterior parietal area V6A, we recently demonstrated the strong presence of depth signals and the extensive convergence of depth and direction information on single neurons during all phases of a fixate-to-reach task in 3-dimensional (3D) space. Using the same task, in the present work we examined the processing of direction and depth information in area PEc of the caudal superior parietal lobule (SPL) in three Macaca fascicularis monkeys. Across the task, depth and direction had a similar, high incidence of modulatory effect. The effect of direction was stronger than depth during the initial fixation period. As the task progressed toward arm movement execution, depth tuning became more prominent than directional tuning and the number of cells modulated by both depth and direction increased significantly. Neurons tuned by depth showed a small bias for far peripersonal space. Cells with directional modulations were more frequently tuned toward contralateral spatial locations, but ipsilateral space was also represented. These findings, combined with results from neighboring areas V6A and PE, support a rostral-to-caudal gradient of overlapping representations for reach depth and direction in SPL. These findings also support a progressive change from visuospatial (vergence angle) to somatomotor representations of 3D space in SPL.

Three-dimensional eye position signals shape both peripersonal space and arm movement activity in the medial posterior parietal cortex

Research conducted over the last decades has established that the medial part of posterior parietal cortex (PPC) is crucial for controlling visually guided actions in human and non-human primates. Within this cortical sector there is area V6A, a crucial node of the parietofrontal network involved in arm movement control in both monkeys and humans. However, the encoding of action-in-depth by V6A cells had been not studied till recently. Recent neurophysiological studies show the existence in V6A neurons of signals related to the distance of targets from the eyes. These signals are integrated, often at the level of single cells, with information about the direction of gaze, thus encoding spatial location in 3D space. Moreover, 3D eye position signals seem to be further exploited at two additional levels of neural processing: (a) in determining whether targets are located in the peripersonal space or not, and (b) in shaping the spatial tuning of arm movement related activity toward reachable targets. These findings are in line with studies in putative homolog regions in humans and together point to a role of medial PPC in encoding both the vergence angle of the eyes and peripersonal space. Besides its role in spatial encoding also in depth, several findings demonstrate the involvement of this cortical sector in non-spatial processes.

Multiple aspects of neural activity during reaching preparation in the medial posterior parietal area v6a

The posterior parietal cortex is involved in the visuomotor transformations occurring during arm-reaching movements. The medial posterior parietal area V6A has been shown to be implicated in reaching execution, but its role in reaching preparation has not been sufficiently investigated. Here, we addressed this issue exploring the neural correlates of reaching preparation in V6A. Neural activity of single cells during the instructed delay period of a foveated Reaching task was compared with the activity in the same delay period during a Detection task. In this latter task, animals fixated the target but, instead of performing an arm reaching movement, they responded with a button release to the go signal. Targets were allocated in different positions in 3-D space. We found three types of neurons: cells where delay activity was equally spatially tuned in the two tasks (Gaze cells), cells spatially tuned only during reaching preparation (Set cells), and cells influenced by both gaze and reaching preparation signals (Gaze/Set cells). In cells influenced by reaching preparation, the delay activity in the Reaching task could be higher or lower compared with the Detection task. All the Set cells and a minority of Gaze/Set cells were more active during reaching preparation. Most cells modulated by movement preparation were also modulated with a congruent spatial tuning during movement execution. Present results highlight the convergence of visuospatial information, reach planning and reach execution signals on V6A, and indicate that visuospatial processing and movement execution have a larger influence on V6A activity than the encoding of reach plans.

Reference frames for reaching when decoupling eye and target position in depth and direction

Spatial representations in cortical areas involved in reaching movements were traditionally studied in a frontoparallel plane where the two-dimensional target location and the movement direction were the only variables to consider in neural computations. No studies so far have characterized the reference frames for reaching considering both depth and directional signals. Here we recorded from single neurons of the medial posterior parietal area V6A during a reaching task where fixation point and reaching targets were decoupled in direction and depth. We found a prevalent mixed encoding of target position, with eye-centered and spatiotopic representations differently balanced in the same neuron. Depth was stronger in defining the reference frame of eye-centered cells, while direction was stronger in defining that of spatiotopic cells. The predominant presence of various typologies of mixed encoding suggests that depth and direction signals are processed on the basis of flexible coordinate systems to ensure optimal motor response.

Long-term sensorimotor adaptation in the ocular following system of primates

The sudden movement of a wide-field image leads to a reflexive eye tracking response referred to as short-latency ocular following. If the image motion occurs soon after a saccade the initial speed of the ocular following is enhanced, a phenomenon known as post-saccadic enhancement. We show in macaque monkeys that repeated exposure to the same stimulus regime over a period of months leads to progressive increases in the initial speeds of ocular following. The improvement in tracking speed occurs for ocular following with and without a prior saccade. As a result of the improvement in ocular following speeds, the influence of post-saccadic enhancement wanes with increasing levels of training. The improvement in ocular following speed following repeated exposure to the same oculomotor task represents a novel form of sensori-motor learning in the context of a reflexive movement.