The dorsal visual stream revisited: Stable circuits or dynamic pathways?

In both macaque and human brain, information regarding visual motion flows from the extrastriate area V6 along two different paths: a dorsolateral one towards areas MT/V5, MST, V3A, and a dorsomedial one towards the visuomotor areas of the superior parietal lobule (V6A, MIP, VIP). The dorsolateral visual stream is involved in many aspects of visual motion analysis, including the recognition of object motion and self motion. The dorsomedial stream uses visual motion information to continuously monitor the spatial location of objects while we are looking and/or moving around, to allow skilled reaching for and grasping of the objects in structured, dynamically changing environments. Grasping activity is present in two areas of the dorsal stream, AIP and V6A. Area AIP is more involved than V6A in object recognition, V6A in encoding vision for action. We suggest that V6A is involved in the fast control of prehension and plays a critical role in biomechanically selecting appropriate postures during reach to grasp behaviors.In everyday life, numerous functional networks, often involving the same cortical areas, are continuously in action in the dorsal visual stream, with each network dynamically activated or inhibited according to the context. The dorsolateral and dorsomedial streams represent only two examples of these networks. Many others streams have been described in the literature, but it is worthwhile noting that the same cortical area, and even the same neurons within an area, are not specific for just one functional property, being part of networks that encode multiple functional aspects. Our proposal is to conceive the cortical streams not as fixed series of interconnected cortical areas in which each area belongs univocally to one stream and is strictly involved in only one function, but as interconnected neuronal networks, often involving the same neurons, that are involved in a number of functional processes and whose activation changes dynamically according to the context

Structural connectivity and functional properties of the macaque superior parietal lobule

Despite the consolidated belief that the macaque superior parietal lobule (SPL) is entirely occupied by Brodmann’s area 5, recent data show that macaque SPL also hosts a large cortical region with structural and functional features similar to that of Brodmann’s area 7. According to these data, the anterior part of SPL is occupied by a somatosensory-dominated cortical region that hosts three architectural and functional distinct regions (PE, PEci, PEip) and the caudal half of SPL by a bimodal somato-visual region that hosts four areas: PEc, MIP, PGm, V6A. To date, the most studied areas of SPL are PE, PEc, and V6A. PE is essentially a high-order somatomotor area, while PEc and V6A are bimodal somatomotor–visuomotor areas, the former with predominant somatosensory input and the latter with predominant visual input. The functional properties of these areas and their anatomical connectivity strongly suggest their involvement in the control of limb movements. PE is suggested to be involved in the preparation/execution of limb movements, in particular, the movements of the upper limb; PEc in the control of movements of both upper and lower limbs, as well as in their interaction with the visual environment; V6A in the control of reach-to-grasp movements performed with the upper limb. In humans, SPL is traditionally considered to have a different organization with respect to macaques. Here, we review several lines of evidence suggesting that this is not the case, showing a similar structure for human and non-human primate SPLs

Anterior-posterior gradient in the integrated processing of forelimb movement direction and distance in macaque parietal cortex

A major issue in modern neuroscience is to understand how cell populations present multiple spatial and motor features during goal-directed movements. The direction and distance (depth) of arm movements often appear to be controlled independently during behavior, but it is unknown whether they share neural resources or not. Using information theory, singular value decomposition, and dimensionality reduction methods, we compare direction and depth effects and their convergence across three parietal areas during an arm movement task. All methods show a stronger direction effect during early movement preparation, whereas depth signals prevail during movement execution. Going from anterior to posterior sectors, we report an increased number of cells processing both signals and stronger depth effects. These findings suggest a serial direction and depth processing consistent with behavioral evidence and reveal a gradient of joint versus independent control of these features in parietal cortex that supports its role in sensorimotor transformations

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

The posterior parietal area V6A: an attentionally-modulated visuomotor region involved in the control of reach-to-grasp action

In the macaque, the posterior parietal area V6A is involved in the control of all phases of reach-to-grasp actions: the transport phase, given that reaching neurons are sensitive to the direction and amplitude of arm movement, and the grasping phase, since reaching neurons are also sensitive to wrist orientation and hand shaping. Reaching and grasping activity are corollary discharges which, together with the somatosensory and visual signals related to the same movement, allow V6A to act as a state estimator that signals discrepancies during the motor act in order to maintain consistency between the ongoing movement and the desired one. Area V6A is also able to encode the target of an action because of gaze-dependent visual neurons and real-position cells. Here, we advance the hypothesis that V6A also uses the spotlight of attention to guide goal-directed movements of the hand, and hosts a priority map that is specific for the guidance of reaching arm movement, combining bottom-up inputs such as visual responses with top-down signals such as reaching plans

Mixed spatial and movement representations in the primate posterior parietal cortex

The posterior parietal cortex (PPC) of humans and non-human primates plays a key role in the sensory and motor transformations required to guide motor actions to objects of interest in the environment. Despite decades of research, the anatomical and functional organization of this region is still a matter of contention. It is generally accepted that specialized parietal subregions and their functional counterparts in the frontal cortex participate in distinct segregated networks related to eye, arm and hand movements. However, experimental evidence obtained primarily from single neuron recording studies in non-human primates has demonstrated a rich mixing of signals processed by parietal neurons, calling into question ideas for a strict functional specialization. Here, we present a brief account of this line of research together with the basic trends in the anatomical connectivity patterns of the parietal subregions. We review, the evidence related to the functional communication between subregions of the PPC and describe progress towards using parietal neuron activity in neuroprosthetic applications. Recent literature suggests a role for the PPC not as a constellation of specialized functional subdomains, but as a dynamic network of sensorimotor loci that combine multiple signals and work in concert to guide motor behavior

Interplay Between Grip and Vision in the Monkey Medial Parietal Lobe

We aimed at understanding the relative contribution of visual information and hand shaping to the neuronal activity of medial posterior parietal area V6A, a newly added area in the monkey cortical grasping circuit. Two Macaca fascicularis performed a Reach-to-Grasp task in the dark and in the light, grasping objects of different shapes. We found that V6A contains Visual cells, activated only during grasping in the light; Motor neurons, equally activated during grasping in the dark and in the light; Visuomotor cells, differently activated while grasping in the dark and in the light. Visual, Motor, and Visuomotor neurons were moderately or highly selective during grasping, whereas they reduced their selectivity during object observation without performing grasping. The use of the same experimental design employed in the dorsolateral grasping area AIP by other authors allowed us to compare the grasp-related properties of V6A and AIP. From these data and from the literature a frame emerges with many similarities between medial grasping area V6A and lateral grasping area AIP: both areas update and control prehension, with V6A less sensitive than AIP to fine visual details of the objects to be grasped, but more involved in coordinating reaching and grasping

Neural coding of action in three dimensions: Task- and time-invariant reference frames for visuospatial and motor-related activity in parietal area V6A

Goal-directed movements involve a series of neural computations that compare the sensory representations of goal location and effector position, and transform these into motor commands. Neurons in posterior parietal cortex (PPC) control several effectors (e.g., eye, hand, foot) and encode goal location in a variety of spatial coordinate systems, including those anchored to gaze direction, and to the positions of the head, shoulder, or hand. However, there is little evidence on whether reference frames depend also on the effector and/or type of motor response. We addressed this issue in macaque PPC area V6A, where previous reports using a fixate-to-reach in depth task, from different starting arm positions, indicated that most units use mixed body/hand-centered coordinates. Here, we applied singular value decomposition and gradient analyses to characterize the reference frames in V6A while the animals, instead of arm reaching, performed a nonspatial motor response (hand lift). We found that most neurons used mixed body/hand coordinates, instead of \u201cpure\u201d body-, or hand-centered coordinates. During the task progress the effect of hand position on activity became stronger compared to target location. Activity consistent with body-centered coding was present only in a subset of neurons active early in the task. Applying the same analyses to a population of V6A neurons recorded during the fixate-to-reach task yielded similar results. These findings suggest that V6A neurons use consistent reference frames between spatial and nonspatial motor responses, a functional property that may allow the integration of spatial awareness and movement control

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

Functional organization of the caudal part of the human superior parietal lobule

: Like in macaque, the caudal portion of the human superior parietal lobule (SPL) plays a key role in a series of perceptive, visuomotor and somatosensory processes. Here, we review the functional properties of three separate portions of the caudal SPL, i.e., the posterior parieto-occipital sulcus (POs), the anterior POs, and the anterior part of the caudal SPL. We propose that the posterior POs is mainly dedicated to the analysis of visual motion cues useful for object motion detection during self-motion and for spatial navigation, while the more anterior parts are implicated in visuomotor control of limb actions. The anterior POs is mainly involved in using the spotlight of attention to guide reach-to-grasp hand movements, especially in dynamic environments. The anterior part of the caudal SPL plays a central role in visually guided locomotion, being implicated in controlling leg-related movements as well as the four limbs interaction with the environment, and in encoding egomotion-compatible optic flow. Together, these functions reveal how the caudal SPL is strongly implicated in skilled visually-guided behaviors