Annalisa Bosco

The Dorsomedial Pathway Is Not Just for Reaching: Grasping Neurons in the Medial Parieto-Occipital Cortex of the Macaque Monkey

Brain control of prehension is thought to rely on two specific brain circuits: a dorsomedial one (involving the areas of the superior parietal lobule and the dorsal premotor cortex) involved in the transport of the hand toward the object and a dorsolateral one (involving the inferior parietal lobule and the ventral premotor cortex) dealing with the preshaping of the hand according to the features of the object. The present study aimed at testing whether a pivotal component of the dorsomedial pathway (area V6A) is involved also in hand preshaping and grip formation to grasp objects of different shapes. Two macaque monkeys were trained to reach and grasp different objects. For each object, animals used a different grip: whole-hand prehension, finger prehension, hook grip, primitive precision grip, and advanced precision grip. Almost half of 235 neurons recorded from V6A displayed selectivity for a grip or a group of grips. Several experimental controls were used to ensure that neural modulation was attributable to grip only. These findings, in concert with previous studies demonstrating that V6A neurons are modulated by reach direction and wrist orientation, that lesion of V6A evokes reaching and grasping deficits, and that dorsal premotor cortex contains both reaching and grasping neurons, indicate that the dorsomedial parieto-frontal circuit may play a central role in all phases of reach-to-grasp action. Our data suggest new directions for the modeling of prehension movements and testable predictions for new brain imaging and neuropsychological experiments.

Hand Orientation during Reach-to-Grasp Movements Modulates Neuronal Activity in the Medial Posterior Parietal Area V6A

Reach-to-grasp actions involve several components of forelimb movements needed to direct the hand toward the object to be grasped, and to orient and preshape the hand according to the object axis and shape. Area V6A, which represents a node of the dorsomedial frontoparietal circuits, has so far been implicated only in directing the arm toward different spatial locations. The present results confirm this finding and demonstrate, for the first time, that during reach-to-grasp, V6A neurons are also modulated by the orientation of the hand. In the present work the object to be grasped was a handle that could have different orientations. Reach-to-grasp movements were executed in complete darkness while gazing at a small fixation point. The majority of the tested cells (76/142; 54%) turned out to be sensitive to the orientation of the handle. Neurons could be modulated during preparation or execution of reach-to-grasp movements. The most represented cells were those modulated by hand orientation both during preparatory and movement periods. These data show that reaching and grasping are processed by the same population of neurons, providing evidence that the coordination of reaching and grasping takes place much earlier than previously thought, i.e., in the parieto-occipital cortex. The data here reported are in agreement with results of lesions to the medial posterior parietal cortex in both monkeys and humans, and with recent imaging data in humans, all of them indicating a functional coupling in the control of reaching and grasping by the medial parietofrontal circuit.

Is the Medial Posterior Parietal Area V6A a Single Functional Area

The visuomotor medial posterior parietal area V6A has been recently subdivided into two cytoarchitectonic sectors called V6Ad and V6Av (Luppino et al., 2005). The aim of the present study was to recognize whether these two cortical sectors show different functional profiles. Fourteen hemispheres from eight animals (Macaca fascicularis) were included in this study, for a total of 3828 extracellularly recorded neurons assigned to areas V6Ad or V6Av on cytoarchitectural basis. The sensitivity of recorded neurons to sensory- and motor-related activities was checked with a series of functional tests performed on behaving animals. We found that cells sensitive to visual stimuli were more represented in V6Av and cells sensitive to somatosensory stimuli were more represented in V6Ad. Visual cells directly encoding spatial locations (real-position cells) were present only in V6Av. Cells encoding basic visual and somatic properties as well as different aspects of reaching and grasping activities were present in both sectors of V6A, although with different incidence. Cells that had reach-related activity enhanced by visual feedback and grasping neurons activated by whole-hand prehension were more concentrated in V6Av. Conversely, reaching neurons inhibited by visual feedback and grasping neurons activated by precision grip were more represented in V6Ad. Although V6Av and V6Ad show partly different functional profiles, our data support the idea that V6A is a single functional area involved in the control of reach-to-grasp movements, with the dorsal sector (V6Ad) more involved in the somatomotor control and the ventral sector (V6Av) in the visual control of reaching and grasping actions.

Vision for Action in the Macaque Medial Posterior Parietal Cortex

Area V6A encodes hand configurations for grasping objects (Fattori et al., 2010). The aim of the present study was to investigate whether V6A cells also encode three-dimensional objects, and the relationship between object encoding and grip encoding. Single neurons were recorded in V6A of two monkeys trained to perform two tasks. In the first task, the monkeys were required to passively view an object without performing any action on it. In the second task, the monkeys viewed an object at the beginning of each trial and then they needed to grasp that object in darkness. Five different objects were used. Both tasks revealed that object presentation activates ∼60% of V6A neurons, with about half of them displaying object selectivity. In the Reach-to-Grasp task, the majority of V6A cells discharged during both object presentation and grip execution, displaying selectivity for either the object or the grip, or in some cases for both object and grip. Although the incidence of neurons encoding grips was twofold that of neurons encoding objects, object selectivity in single cells was as strong as grip selectivity, indicating that V6A cells were able to discriminate both the different objects and the different grips required to grasp them. Hierarchical cluster analysis revealed that clustering of the object-selective responses depended on the task requirements (view only or view to grasp) and followed a visual or a visuomotor rule, respectively. Object encoding in V6A reflects representations for action, useful for motor control in reach-to-grasp.

Reaching Activity in the Medial Posterior Parietal Cortex of Monkeys Is Modulated by Visual Feedback

Reaching and grasping an object is an action that can be performed in light, as well as in darkness. Area V6A is a visuomotor area of the medial posterior parietal cortex involved in the control of reaching movements. It contains reaching neurons as well as neurons modulated by passive somatosensory and visual stimulations. In the present work we analyze the effect of visual feedback on reaching activity of V6A neurons. Three macaques were trained to execute reaching movements in two conditions: in darkness, where only the reaching target was visible, and in full light, where the monkey also saw its own moving arm and the environment. Approximately 85% of V6A neurons (127/149) were significantly related to the task in at least one of the two conditions. The majority of task-related cells (69%) showed reach-related activity in both visual conditions, some were modulated only in light (15%), while others only in dark (16%). The sight of the moving arm often changed dramatically the cells response to arm movements. In some cases the reaching activity was enhanced and in others it was reduced or disappeared altogether. These neuronal properties may represent differences in the degree to which cells are influenced by feedback control versus feedforward movement planning. On average, reach-related modulations were stronger in light than in dark, a phenomenon similar to that observed in brain imaging experiments in the human medial posterior parietal cortex, a region likely homologous to macaque area V6A.

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.

Covert Shift of Attention Modulates the Ongoing Neural Activity in a Reaching Area of the Macaque Dorsomedial Visual Stream

Background Attention is used to enhance neural processing of selected parts of a visual scene. It increases neural responses to stimuli near target locations and is usually coupled to eye movements. Covert attention shifts, however, decouple the attentional focus from gaze, allowing to direct the attention to a peripheral location without moving the eyes. We tested whether covert attention shifts modulate ongoing neuronal activity in cortical area V6A, an area that provides a bridge between visual signals and arm-motor control. Methodology/Principal Findings We performed single cell recordings from 3 Macaca Fascicularis trained to fixate straight-head, while shifting attention outward to a peripheral cue and inward again to the fixation point. We found that neurons in V6A are influenced by spatial attention. The attentional modulation occurs without gaze shifts and cannot be explained by visual stimulations. Visual, motor, and attentional responses can occur in combination in single neurons. Conclusions/Significance This modulation in an area primarily involved in visuo-motor transformation for reaching may form a neural basis for coupling attention to the preparation of reaching movements. Our results show that cortical processes of attention are related not only to eye-movements, as many studies have shown, but also to arm movements, a finding that has been suggested by some previous behavioral findings. Therefore, the widely-held view that spatial attention is tightly intertwined with—and perhaps directly derived from—motor preparatory processes should be extended to a broader spectrum of motor processes than just eye movements.

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.

Vision for Prehension in the Medial Parietal Cortex

Abstract In the last 2 decades, the medial posterior parietal area V6A has been extensively studied in awake macaque monkeys for visual and somatosensory properties and for its involvement in encoding of spatial parameters for reaching, including arm movement direction and amplitude. This area also contains populations of neurons sensitive to grasping movements, such as wrist orientation and grip formation. Recent work has shown that V6A neurons also encode the shape of graspable objects and their affordance. In other words, V6A seems to encode object visual properties specifically for the purpose of action, in a dynamic sequence of visuomotor transformations that evolve in the course of reach‐to‐grasp action. We propose a model of cortical circuitry controlling reach‐to‐grasp actions, in which V6A acts as a comparator that monitors differences between current and desired hand positions and configurations. This error signal could be used to continuously update the motor output, and to correct reach direction, hand orientation, and/or grip aperture as required during the act of prehension. In contrast to the generally accepted view that the dorsomedial component of the dorsal visual stream encodes reaching, but not grasping, the functional properties of V6A neurons strongly suggest the view that this area is involved in encoding all phases of prehension, including grasping.