Anterior Intraparietal Research Articles

On the Neurocognitive Co-Evolution of Tool Behavior and Language: Insights from the Massive Redeployment Framework.

Understanding the link between brain evolution and the evolution of distinctive features of modern human cognition is a fundamental challenge. A still unresolved question concerns the co-evolution of tool behavior (i.e., tool use or tool making) and language. The shared neurocognitive processes hypothesis suggests that the emergence of the combinatorial component of language skills within the frontal lobe/Broca's area made possible the complexification of tool-making skills. The importance of the frontal lobe/Broca's area in tool behavior is somewhat surprising with regard to the literature on neuropsychology and cognitive neuroscience, which has instead stressed the critical role of the left inferior parietal lobe. Therefore, to be complete, any version of the shared neurocognitive processes hypothesis needs to integrate the potential interactions between the frontal lobe/Broca's area and the left inferior parietal lobe as well as their co-evolution at a phylogenetic level. Here, we sought to provide the first elements of answer through the use of the massive deployment framework, which posits that evolutionarily older brain areas are deployed in more cognitive functions (i.e., they are less specific). We focused on the left parietal cortex, and particularly the left areas PF, PGI, and anterior intraparietal (AIP), which are known to be involved in tool use, language, and motor control, respectively. The deployment of each brain area in different cognitive functions was measured by conducting a meta-analysis of neuroimaging studies. Our results confirmed the pattern of specificity for each brain area and also showed that the left area PGI was far less specific than the left areas PF and AIP. From these findings, we discuss the different evolutionary scenarios depicting the potential co-evolution of the combinatorial and generative components of language and tool behavior in our lineage.

Anterior Intraparietal Area: A Hub in the Observed Manipulative Action Network.

Current knowledge regarding the processing of observed manipulative actions (OMAs) (e.g., grasping, dragging, or dropping) is limited to grasping and underlying neural circuitry remains controversial. Here, we addressed these issues by combining chronic neuronal recordings along the anteroposterior extent of monkeys’ anterior intraparietal (AIP) area with tracer injections into the recorded sites. We found robust neural selectivity for 7 distinct OMAs, particularly in the posterior part of AIP (pAIP), where it was associated with motor coding of grip type and own-hand visual feedback. This cluster of functional properties appears to be specifically grounded in stronger direct connections of pAIP with the temporal regions of the ventral visual stream and the prefrontal cortex, as connections with skeletomotor related areas and regions of the dorsal visual stream exhibited opposite or no rostrocaudal gradients. Temporal and prefrontal areas may provide visual and contextual information relevant for manipulative action processing. These results revise existing models of the action observation network, suggesting that pAIP constitutes a parietal hub for routing information about OMA identity to the other nodes of the network.

Decoding Grasping Movements from the Parieto-Frontal Reaching Circuit in the Nonhuman Primate

Prehension movements typically include a reaching phase, guiding the hand toward the object, and a grip phase, shaping the hand around it. The dominant view posits that these components rely upon largely independent parieto-frontal circuits: a dorso-medial circuit involved in reaching and a dorso-lateral circuit involved in grasping. However, mounting evidence suggests a more complex arrangement, with dorso-medial areas contributing to both reaching and grasping. To investigate the role of the dorso-medial reaching circuit in grasping, we trained monkeys to reach-and-grasp different objects in the dark and determined if hand configurations could be decoded from functional magnetic resonance imaging (MRI) responses obtained from the reaching and grasping circuits. Indicative of their established role in grasping, object-specific grasp decoding was found in anterior intraparietal (AIP) area, inferior parietal lobule area PFG and ventral premotor region F5 of the lateral grasping circuit, and primary motor cortex. Importantly, the medial reaching circuit also conveyed robust grasp-specific information, as evidenced by significant decoding in parietal reach regions (particular V6A) and dorsal premotor region F2. These data support the proposed role of dorso-medial "reach" regions in controlling aspects of grasping and demonstrate the value of complementing univariate with more sensitive multivariate analyses of functional MRI (fMRI) data in uncovering information coding in the brain.

Decoding a wide range of hand configurations from macaque motor, premotor, and parietal cortices.

Despite recent advances in decoding cortical activity for motor control, the development of hand prosthetics remains a major challenge. To reduce the complexity of such applications, higher cortical areas that also represent motor plans rather than just the individual movements might be advantageous. We investigated the decoding of many grip types using spiking activity from the anterior intraparietal (AIP), ventral premotor (F5), and primary motor (M1) cortices. Two rhesus monkeys were trained to grasp 50 objects in a delayed task while hand kinematics and spiking activity from six implanted electrode arrays (total of 192 electrodes) were recorded. Offline, we determined 20 grip types from the kinematic data and decoded these hand configurations and the grasped objects with a simple Bayesian classifier. When decoding from AIP, F5, and M1 combined, the mean accuracy was 50% (using planning activity) and 62% (during motor execution) for predicting the 50 objects (chance level, 2%) and substantially larger when predicting the 20 grip types (planning, 74%; execution, 86%; chance level, 5%). When decoding from individual arrays, objects and grip types could be predicted well during movement planning from AIP (medial array) and F5 (lateral array), whereas M1 predictions were poor. In contrast, predictions during movement execution were best from M1, whereas F5 performed only slightly worse. These results demonstrate for the first time that a large number of grip types can be decoded from higher cortical areas during movement preparation and execution, which could be relevant for future neuroprosthetic devices that decode motor plans.

The neural basis of human tool use.

In this review, we propose that the neural basis for the spontaneous, diversified human tool use is an area devoted to the execution and observation of tool actions, located in the left anterior supramarginal gyrus (aSMG). The aSMG activation elicited by observing tool use is typical of human subjects, as macaques show no similar activation, even after an extensive training to use tools. The execution of tool actions, as well as their observation, requires the convergence upon aSMG of inputs from different parts of the dorsal and ventral visual streams. Non-semantic features of the target object may be provided by the posterior parietal cortex (PPC) for tool-object interaction, paralleling the well-known PPC input to anterior intraparietal (AIP) for hand-object interaction. Semantic information regarding tool identity, and knowledge of the typical manner of handling the tool, could be provided by inferior and middle regions of the temporal lobe. Somatosensory feedback and technical reasoning, as well as motor and intentional constraints also play roles during the planning of tool actions and consequently their signals likewise converge upon aSMG. We further propose that aSMG may have arisen though duplication of monkey AIP and invasion of the duplicate area by afferents from PPC providing distinct signals depending on the kinematics of the manipulative action. This duplication may have occurred when Homo Habilis or Homo Erectus emerged, generating the Oldowan or Acheulean Industrial complexes respectively. Hence tool use may have emerged during hominid evolution between bipedalism and language. We conclude that humans have two parietal systems involved in tool behavior: a biological circuit for grasping objects, including tools, and an artifactual system devoted specifically to tool use. Only the latter allows humans to understand the causal relationship between tool use and obtaining the goal, and is likely to be the basis of all technological developments.

Coding of Shape Features in the Macaque Anterior Intraparietal Area

The exquisite ability of primates to grasp and manipulate objects relies on the transformation of visual information into motor commands. To this end, the visual system extracts object affordances that can be used to program and execute the appropriate grip. The macaque anterior intraparietal (AIP) area has been implicated in the extraction of affordances for the purpose of grasping. Neurons in the AIP area respond during visually guided grasping and to the visual presentation of objects. A subset of AIP neurons is also activated by two-dimensional images of objects and even by outline contours defining the object shape, but it is unknown how AIP neurons actually represent object shape. In this study, we used a stimulus reduction approach to determine the minimum effective shape feature evoking AIP responses. AIP neurons responding to outline shapes also responded selectively to very small fragment stimuli measuring only 1-2°. This fragment selectivity could not be explained by differences in eye movements or simple orientation selectivity, but proved to be highly dependent on the relative position of the stimulus in the receptive field. Our findings challenge the current understanding of the AIP area as a critical stage in the dorsal stream for the extraction of object affordances.

Perturbing the Action Observation Network During Perception and Categorization of Actions' Goals and Grips: State-Dependency and Virtual Lesion TMS Effects

Watching others grasping and using objects activates an action observation network (AON), including inferior frontal (IFC), anterior intraparietal (AIP), and somatosensory cortices (S1). Yet, causal evidence of the differential involvement of such AON sensorimotor nodes in representing high- and low-level action components (i.e., end-goals and grip type) is meager. To address this issue, we used transcranial magnetic stimulation-adaptation (TMS-A) during 2 novel action perception tasks. Participants were shown adapting movies displaying a demonstrator performing goal-directed actions with a tool, using either power or precision grips. They were then asked to match the end-goal (Goal-recognition task) or the grip (Grip-recognition task) of actions shown in test pictures to the adapting movies. TMS was administered over IFC, AIP, or S1 during presentation of test pictures. Virtual lesion-like effects were found in the Grip-recognition task where IFC stimulation induced a general performance decrease, suggesting a critical role of IFC in perceiving grips. In the Goal-recognition task, IFC and S1 stimulation differently affected the processing of "adapted" and "nonadapted" goals. These "state-dependent" effects suggest that the overall goal of seen actions is encoded into functionally distinct and spatially overlapping neural populations in IFC-S1 and such encoding is critical for recognizing and understanding end-goals.

Reach and Gaze Representations in Macaque Parietal and Premotor Grasp Areas

Voluntary movements are frequently composed of several actions that are combined to achieve a specific behavior. For example, prehension involves reaching and grasping actions to transport the hand to a target to grasp or manipulate it. For controlling these actions, separate parietofrontal networks have been described for generating reaching and grasping actions. However, this separation has been challenged recently for the dorsomedial part of this network (area V6A). Here we report that the anterior intraparietal (AIP) and the rostral ventral premotor area (F5) in the macaque, which are both part of the dorsolateral parietofrontal network and causally linked to hand grasping movements, also represent spatial information during the execution of a reach-to-grasp task. In addition to grip type information, gaze and target positions were represented in AIP and F5 and could be readily decoded from single unit activity in these areas. Whereas the fraction of grip type tuned units increased toward movement execution, the number of cells with spatial representations stayed relatively constant throughout the task, although more prominently in AIP than in F5. Furthermore, the recorded target position signals were substantially encoded in retinotopic coordinates. In conclusion, the simultaneous presence of grasp-related and spatial information in AIP and F5 suggests at least a supportive role of these spatial signals for the planning of grasp actions. Whether these spatial signals in AIP and F5 also play a causal role for the planning of reach actions would need to be the subject of further investigations.

Anatomical Evidence for the Involvement of the Macaque Ventrolateral Prefrontal Area 12r in Controlling Goal-Directed Actions

The macaque ventrolateral prefrontal (VLPF) area 12r is thought to be involved in higher-order nonspatial information processing. We found that this area is connectionally heterogeneous, and the intermediate part is fully integrated in a cortical network involved in selecting and controlling object-oriented hand and mouth actions. Specifically, intermediate area 12r displayed dense connections with the caudal half of area 46v and orbitofrontal areas and relatively strong extraprefrontal connections involving the following: (1) the hand- and mouth-related ventral premotor area F5 and the anterior intraparietal (AIP) area, jointly involved in visuomotor transformations for grasping; (2) the SII sector that is connected to AIP and F5; (3) a sector of the inferotemporal area TEa/m, primarily corresponding to the sector densely connected to AIP; and (4) the insular and opercular frontal sectors, which are connected to AIP and F5. This connectivity pattern differed markedly from those of the caudal and rostral parts of area 12r. Caudal area 12r displayed dense connections with the caudal part of the VLPF, including oculomotor areas 8/FEF and 45B, relatively weak orbitofrontal connections and extraprefrontal connections limited to the inferotemporal cortex. Rostral area 12r displayed connections mostly with rostral prefrontal and orbitofrontal areas and relatively weaker connections with the fundus and the upper bank of the superior temporal sulcus. The present data suggest that the intermediate part of area 12r is involved in nonspatial information processing related to object properties and identity, for selecting and controlling goal-directed hand and mouth actions.

Action Observation Circuits in the Macaque Monkey Cortex

In both monkeys and humans, the observation of actions performed by others activates cortical motor areas. An unresolved question concerns the pathways through which motor areas receive visual information describing motor acts. Using functional magnetic resonance imaging (fMRI), we mapped the macaque brain regions activated during the observation of grasping actions, focusing on the superior temporal sulcus region (STS) and the posterior parietal lobe. Monkeys viewed either videos with only the grasping hand visible or videos with the whole actor visible. Observation of both types of grasping videos activated elongated regions in the depths of both lower and upper banks of STS, as well as parietal areas PFG and anterior intraparietal (AIP). The correlation of fMRI data with connectional data showed that visual action information, encoded in the STS, is forwarded to ventral premotor cortex (F5) along two distinct functional routes. One route connects the upper bank of the STS with area PFG, which projects, in turn, to the premotor area F5c. The other connects the anterior part of the lower bank of the STS with premotor areas F5a/p via AIP. Whereas the first functional route emphasizes the agent and may relay visual information to the parieto-frontal mirror circuit involved in understanding the agent's intentions, the second route emphasizes the object of the action and may aid in understanding motor acts with respect to their immediate goal.

A Distinct Representation of Three-Dimensional Shape in Macaque Anterior Intraparietal Area: Fast, Metric, and Coarse

Differences in the horizontal positions of retinal images--binocular disparity--provide important cues for three-dimensional object recognition and manipulation. We investigated the neural coding of three-dimensional shape defined by disparity in anterior intraparietal (AIP) area. Robust selectivity for disparity-defined slanted and curved surfaces was observed in a high proportion of AIP neurons, emerging at relatively short latencies. The large majority of AIP neurons preserved their three-dimensional shape preference over different positions in depth, a hallmark of higher-order disparity selectivity. Yet both stimulus type (concave-convex) and position in depth could be reliably decoded from the AIP responses. The neural coding of three-dimensional shape was based on first-order (slanted surfaces) and second-order (curved surfaces) disparity selectivity. Many AIP neurons tolerated the presence of disparity discontinuities in the stimulus, but the population of AIP neurons provided reliable information on the degree of curvedness of the stimulus. Finally, AIP neurons preserved their three-dimensional shape preference over different positions in the frontoparallel plane. Thus, AIP neurons extract or have access to three-dimensional object information defined by binocular disparity, consistent with previous functional magnetic resonance imaging data. Unlike the known representation of three-dimensional shape in inferior temporal cortex, the neural representation in AIP appears to emphasize object parameters required for the planning of grasping movements.

Functional Imaging of the Parietal Cortex during Action Execution and Observation

We used the (14)C-deoxyglucose method to map the functional activity in the cortex of the lateral and medial parietal convexity, the intraparietal and the parietoccipital sulci of monkeys which either reached and grasped a 3D-object or observed the same reaching-to-grasp movements executed by a human. Execution of reaching-to-grasp induced activations in the superior parietal areas SI-forelimb/convexity, PE, PE caudal (PEc); in the intraparietal areas PE intraparietal (PEip), medial intraparietal (MIP), 5 intraparietal posterior, ventral intraparietal (VIP), anterior intraparietal (AIP), lateral intraparietal dorsal; in the inferior parietal areas PF, PFG, PG; in the parietoccipital areas V6, V6A-dorsal; in the medial cortical areas PGm/7m and retrosplenial cortex. Observation of reaching-to-grasp activated areas SI-forelimb/convexity, PE lateral, PEc, PEip, MIP, VIP, AIP, PF, V6, PGm/7m, 31, and retrosplenial cortex. The common activations were stronger for execution than for observation and the interhemispheric differences were smaller for observation than for execution, contributing to the attribution of action to the correct agent. The extensive overlap of parietal networks activated for action execution and observation supports the "mental simulation theory" which assigns the role of understanding others' actions to the entire distributed neural network responsible for the execution of actions, and not the concept of "mirroring" which reflects the function of a certain class of cells in a couple of cortical areas.

Cortical Connections of the Macaque Anterior Intraparietal (AIP) Area

We traced the cortical connections of the anterior intraparietal (AIP) area, which is known to play a crucial role in visuomotor transformations for grasping. AIP displayed major connections with 1) areas of the inferior parietal lobule convexity, the rostral part of the lateral intraparietal area and the SII region; 2) ventral visual stream areas of the lower bank of the superior temporal sulcus and the middle temporal gyrus; and 3) the premotor area F5 and prefrontal areas 46 and 12. Additional connections were observed with the caudal intraparietal area and the ventral part of the frontal eye field. This study suggests that visuomotor transformations for object-oriented actions, processed in AIP, rely not only on dorsal visual stream information related to the object's physical properties but also on ventral visual stream information related to object identity. The identification of direct anatomical connections with the inferotemporal cortex suggests that AIP also has a unique role in linking the parietofrontal network of areas involved in sensorimotor transformations for grasping with areas involved in object recognition. Thus, AIP could represent a crucial node in a cortical circuit in which hand-related sensory and motor signals gain access to representations of object identity for tactile object recognition.

The role of parietal cortex in visuomotor control: What have we learned from neuroimaging?

Research from macaque neurophysiology and human neuropsychology has implicated the parietal cortex in the sensory control of action. Functional neuroimaging has been very valuable in localizing and characterizing specific regions of the human brain involved in visuomotor actions involving different effectors, such as the eyes, head, arms and hands. Here, we review the areas discovered by human neuroimaging, including the putative functional equivalents of the following macaque regions: parietal eye fields (PEF), ventral intraparietal (VIP) area, parietal reach region (PRR) and the anterior intraparietal (AIP) area. We discuss the challenges of studying realistic movements in the imaging environment, the lateralization of visuomotor function, caveats involved in proposing interspecies homologies and the limitations and future directions for neuroimaging studies of visuomotor control.

Action selectivity in parietal and temporal cortex

The sensory–action theory proposes that the neural substrates underlying action representations are related to a visuomotor action system encompassing the left ventral premotor cortex, the anterior intraparietal (AIP) and left posterior middle temporal gyrus (LPMT). Using fMRI, we demonstrate that semantic decisions on action, relative to non-action words, increased activation in the left AIP and LPMT irrespective of whether the words were presented in a written or spoken form. Left AIP and LPMT might thus play the role of amodal semantic regions that can be activated via auditory as well as visual input. Left AIP and LPMT did not distinguish between different types of actions such as hand actions and whole body movements, although a right STS region responded selectively to whole body movements.

Visually guided grasping produces fMRI activation in dorsal but not ventral stream brain areas

Although both reaching and grasping require transporting the hand to the object location, only grasping also requires processing of object shape, size and orientation to preshape the hand. Behavioural and neuropsychological evidence suggests that the object processing required for grasping relies on different neural substrates from those mediating object recognition. Specifically, whereas object recognition is believed to rely on structures in the ventral (occipitotemporal) stream, object grasping appears to rely on structures in the dorsal (occipitoparietal) stream. We used functional magnetic resonance imaging (fMRI) to determine whether grasping (compared to reaching) produced activation in dorsal areas, ventral areas, or both. We found greater activity for grasping than reaching in several regions, including anterior intraparietal (AIP) cortex. We also performed a standard object perception localizer (comparing intact vs. scrambled 2D object images) in the same subjects to identify the lateral occipital complex (LOC), a ventral stream area believed to play a critical role in object recognition. Although LOC was activated by the objects presented on both grasping and reaching trials, there was no greater activity for grasping compared to reaching. These results suggest that dorsal areas, including AIP, but not ventral areas such as LOC, play a fundamental role in computing object properties during grasping.

Neural mechanisms of visual guidance of hand action in the parietal cortex of the monkey.

We studied the functional properties of the hand manipulation task-related neurons (N = 136) in the posterior bank of the intraparietal sulcus (IPS) using four kinds of objects for manipulation. We performed cluster analysis by comparing the profiles of activity of these neurons across objects during manipulation in the light, and classified them into nine groups, four highly selective, four moderately selective, and one nonselective group. Activity profiles of these neurons across objects were analyzed in four task conditions: object manipulation and object fixation both in the light and in the dark. Cells were classified as "motor-dominant," "visual-dominant," and "visual and motor" neurons, and the latter two were further subdivided into object type and non-object type. Most of the highly selective neurons (35 of 136) preferred the same object for manipulation in the dark as in the light. The object type "visual and motor" neurons preferred the same object for manipulation and fixation, suggesting that these neurons play an important role in matching the pattern of hand movement to the visuo-spatial characteristics of the object to be manipulated. A large majority of highly selective hand manipulation neurons were localized in the rostral part of the posterior bank of IPS, which we designated as the anterior intraparietal (AIP) area. We propose a conceptual model of the system for visual guidance of hand action including parietal hand manipulation neurons.