Claustral Input to the Macaque Medial Posterior Parietal Cortex (Superior Parietal Lobule and Adjacent Areas).

The projections from the claustrum to cortical areas within and adjacent to the superior parietal lobule were studied in 10 macaque monkeys, using retrograde tracers, computerized reconstructions, and quantitative methods. In contrast with the classical view that posterior parietal areas receive afferents primarily from the dorsal and posterior regions of the claustrum, we found that these areas receive more extensive projections, including substantial afferents from the anterior and ventral regions of the claustrum. Moreover, our findings uncover a previously unsuspected variability in the precise regions of the claustrum that originate the projections, according to the target areas. For example, areas dominated by somatosensory inputs for control of body movements tend to receive most afferents from the dorsal-posterior claustrum, whereas those which also receive significant visual inputs tend to receive more afferents from the ventral claustrum. In addition, different areas within these broadly defined groups differ in terms of quantitative emphasis in the origin of projections. Overall, these results argue against a simple model whereby adjacency in the cortex determines adjacency in the sectors of claustral origin of projections and indicate that subnetworks defined by commonality of function may be an important factor in defining claustrocortical topography.

The superior parietal lobule of primates: a sensory-motor hub for interaction with the environment.

The superior parietal lobule of the macaque monkey occupies the postero-medial part of the parietal lobe and plays a crucial role in the integration of different sources of information (from visual, motor and somatosensory brain regions) for the purpose of high-level cognitive functions, as perception for action. This region encompasses the intraparietal sulcus and the parieto-occipital sulcus and includes also the precuneate cortex in the mesial surface of the hemisphere. It hosts several areas extensively studied in the macaque: PE, PEip, PEci anteriorly and PEc, MIP, PGm and V6A posteriorly. Recently studies based on functional MRI have suggested putative human homologue of some of the areas of the macaque superior parietal lobule. Here we review the anatomical subdivision, the cortico-cortical and thalamo-cortical connections of the macaque superior parietal lobule compared with their functional properties and the homology with human organization in physiological and lesioned situations. The knowledge of this part of the macaque brain could help in understanding pathological conditions that in humans affect the normal behaviour of arm-reaching actions and can inspire brain computer interfaces performing in more accurate ways the sensorimotor transformations needed to interact with the surrounding environment.

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.

Uniformity and Diversity of Cortical Projections to Precuneate Areas in the Macaque Monkey: What Defines Area PGm?

We report on the corticocortical connections of areas on the mesial surface of the macaque posterior parietal cortex, based on 10 retrograde tracer injections targeting different parts of the precuneate gyrus. Analysis of afferent connections supported the existence of two areas: PGm (also known as 7 m) and area 31. Both areas received major afferents from the V6A complex and from the external subdivision of area 23, but they differed in most other aspects. Area 31 showed greater emphasis on connections with premotor and parietal sensorimotor areas, whereas PGm received a greater proportion of its afferents from visuomotor structures involved in spatial cognition (including the lateral intraparietal cortex, inferior parietal lobule, and the putative visual areas in the ventral part of the precuneus). Medially, the anterior cingulate cortex (area 24) preferentially targeted area 31, whereas retrosplenial areas preferentially targeted PGm. These results indicate that earlier views on the connections of PGm were based on tracer injections that included parts of adjacent areas (including area 31), and prompt a reassessment of the limits of PGm. Our findings are compatible with a primary role of PGm in visuospatial cognition (including navigation), while supporting a role for area 31 in sensorimotor planning and coordination.

Vision for Prehension in the Medial Parietal Cortex.

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.

Object affordance modulates visual responses in the macaque medial posterior parietal cortex.

Area V6A is a visuomotor area of the dorsomedial visual stream that contains cells modulated by object observation and by grip formation. As different objects have different shapes but also evoke different grips, the response selectivity during object presentation could reflect either the coding of object geometry or object affordances. To clarify this point, we here investigate neural responses of V6A cells when monkeys observed two objects with similar visual features but different contextual information, such as the evoked grip type. We demonstrate that many V6A cells respond to the visual presentation of objects and about 30% of them by the object affordance. Given that area V6A is an early stage in the visuomotor processes underlying grasping, these data suggest that V6A may participate in the computation of object affordances. These results add some elements in the recent literature about the role of the dorsal visual stream areas in object representation and contribute in elucidating the neural correlates of the extraction of action-relevant information from general object properties, in agreement with recent neuroimaging studies on humans showing that vision of graspable objects activates action coding in the dorsomedial visual steam.

The medial parietal occipital areas in the macaque monkey.

The number, location, extent, and functional properties of the cortical areas that occupy the medial parieto-occipital cortex (mPOC) have been, and still is, a matter of scientific debate. The mPOC is a convoluted region of the brain that presents a high level of individual variability, and the fact that many areas of mPOC are located within very deep sulci further limits the possibility to investigate their anatomo-functional properties. In the present review, we summarize the location and extent of mPOC areas in the macaque brain as obtained by architectural, connectional, and functional data. The different approaches lead to a subdivision of mPOC that includes areas V2, V3, V6, V6Av, and V6Ad. Extrastriate areas V2 and V3 occupy the posterior wall of the parieto-occipital sulcus (POs). The fundus of POs and the ventralmost part of the anterior wall of the sulcus are occupied by a retinotopically organized visual area, called V6, which represents the contralateral part of the visual field and emphasizes its periphery. The remaining part of the anterior wall of POs is occupied by two areas, V6Av and V6Ad, which contain visual as well as arm reaching neurons. Our analyses suggest that areas V6 and V6Av, together, occupy the cortical territory previously described as area PO. Functionally, area V6 is a motion area particularly sensitive to the real motion of objects in the animal's field of view, while V6Av and V6Ad are visuomotor areas likely involved in the visual guidance of arm movement and object prehension.

Cortical connectivity suggests a role in limb coordination for macaque area PE of the superior parietal cortex.

In macaques, superior parietal lobule area 5 has been described as occupying an extensive region, which includes the caudal half of the postcentral convexity as well as the medial bank of the intraparietal sulcus. Modern neuroanatomical methods have allowed the identification of various areas within this region. In the present study, we investigated the corticocortical afferent projections of one of these subdivisions, area PE. Our results demonstrate that PE, defined as a single architectonic area that contains a topographic map of the body, forms specific connections with somatic and motor fields. Thus, PE receives major afferents from parietal areas, mainly area 2, PEc, several areas in the medial bank of the intraparietal sulcus, opercular areas PGop/PFop, and the retroinsular area, frontal afferents from the primary motor cortex, the supplementary motor area, and the caudal subdivision of dorsal premotor cortex, as well as afferents from cingulate areas PEci, 23, and 24. The presence and relative strength of these connections depend on the location of injection sites, so that lateral PE receives preferential input from anterior sectors of the medial bank of intraparietal sulcus and from the ventral premotor cortex, whereas medial PE forms denser connections with area PEc and motor fields. In contrast with other posterior parietal areas, there are no projections to PE from occipital or prefrontal cortices. Overall, the sensory and motor afferents to PE are consistent with functions in goal-directed movement but also hint at a wider variety of motor coordination roles.

Visual sensitivity at the service of action control in posterior parietal cortex.

The posterior parietal cortex (PPC) serves as a crucial hub for the integration of sensory with motor cues related to voluntary actions. Visual input is used in different ways along the dorsomedial and the dorsolateral visual pathways. Here we focus on the dorsomedial pathway and recognize a visual representation at the service of action control. Employing different experimental paradigms applied to behaving monkeys while single neural activity is recorded from the medial PPC (area V6A), we show how plastic visual representation can be, matching the different contexts in which the same object is proposed. We also present data on the exchange between vision and arm actions and highlight how this rich interplay can be used to weight different sensory inputs in order to monitor and correct arm actions online. Indeed, neural activity during reaching or reach-to-grasp actions can be excited or inhibited by visual information, suggesting that the visual perception of action, rather than object recognition, is the most effective factor for area V6A. Also, three-dimensional object shape is encoded dynamically by the neural population, according to the behavioral context of the monkey. Along this line, mirror neuron discharges in V6A indicate the plasticity of visual representation of the graspable objects, that changes according to the context and peaks when the object is the target of one's own action. In other words, object encoding in V6A is a visual encoding for action.

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.

Cortical connections of area V6Av in the macaque: a visual-input node to the eye/hand coordination system.

The goal of the present study was to elucidate the corticocortical afferent connections of area V6Av, the ventral subregion of area V6A, using retrograde neuronal tracers combined with physiological and cytoarchitectonic analyses in the macaque monkey. The results revealed that V6Av receives many of its afferents from extrastriate area V6, and from regions of areas V2, V3, and V4 subserving peripheral vision. Additional extrastriate visual projections originate in dorsal stream areas MT and MST. Area V6Av does not receive projections directly from V1; such connections were only observed when the injection sites crossed into area V6. The strongest parietal lobe afferents originate in fields V6Ad, PGm, MIP (medial intraparaietal), and PG, with frontal lobe afferents originating from the frontal eye field, caudal area 46, and the rostral subdivision of the dorsal premotor area (F7). A comparison of their respective connections supports the view that V6Av is functionally distinct from adjacent areas (V6 and V6Ad). The strong afferents from V6 and other extrastriate areas are consistent with physiological data that suggest that V6Av is primarily a visual area, supporting the notion that V6Av is part of a dorsomedial cortical network performing fast form and motion analyses needed for the visual guidance of action.

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.

Cortical connections of parietal field PEc in the macaque: linking vision and somatic sensation for the control of limb action.

The cortical projections to the caudal part of the superior parietal lobule (area PEc) were studied in 6 cynomolgus monkeys using fluorescence tracers. Significant numbers of labeled cells were found in a restricted network of parietal, mesial, and frontal areas. Quantitative analysis demonstrated that approximately 30% of the total projection neurons originated in the adjacent areas of the dorsocaudal part of the superior parietal lobule (areas PE and V6A). The medial bank of the intraparietal sulcus, inferior parietal lobule, and frontal lobe (mainly the dorsocaudal part of premotor area F2) each contributed approximately 15% of the projection neurons. About 15% of the labeled neurons were located in the posterior cingulate area (PEci) and another 10% in other areas of the mesial surface of the hemisphere. Based on these data, we suggest that PEc processes information about the position of the limbs. The specific anatomical links between PEc and motor and premotor areas that host a representation of the lower limbs, together with the link with vestibular cortex and with areas involved in the analysis of optic flow and spatial navigation, imply a role for PEc in locomotion and coordinated limb movement in the environment.

Vision for action: thalamic and cortical inputs to the macaque superior parietal lobule.

The dorsal visual stream, the cortical circuit that in the primate brain is mainly dedicated to the visual control of actions, is split into two routes, a lateral and a medial one, both involved in coding different aspects of sensorimotor control of actions. The lateral route, named "lateral grasping network", is mainly involved in the control of the distal part of prehension, namely grasping and manipulation. The medial route, named "reach-to-grasp network", is involved in the control of the full deployment of prehension act, from the direction of arm movement to the shaping of the hand according to the object to be grasped. In macaque monkeys, the reach-to-grasp network (the target of this review) includes areas of the superior parietal lobule (SPL) that hosts visual and somatosensory neurons well suited to control goal-directed limb movements toward stationary as well as moving objects. After a brief summary of the neuronal functional properties of these areas, we will analyze their cortical and thalamic inputs thanks to retrograde neuronal tracers separately injected into the SPL areas V6, V6A, PEc, and PE. These areas receive visual and somatosensory information distributed in a caudorostral, visuosomatic trend, and some of them are directly connected with the dorsal premotor cortex. This review is particularly focused on the origin and type of visual information reaching the SPL, and on the functional role this information can play in guiding limb interaction with objects in structured and dynamic environments.

Connections of the dorsomedial visual area: pathways for early integration of dorsal and ventral streams in extrastriate cortex.

The dorsomedial area (DM), a subdivision of extrastriate cortex characterized by heavy myelination and relative emphasis on peripheral vision, remains the least understood of the main targets of striate cortex (V1) projections in primates. Here we placed retrograde tracer injections encompassing the full extent of this area in marmoset monkeys, and performed quantitative analyses of the numerical strengths and laminar patterns of its afferent connections. We found that feedforward projections from V1 and from the second visual area (V2) account for over half of the inputs to DM, and that the vast majority of the remaining connections come from other topographically organized visual cortices. Extrastriate projections to DM originate in approximately equal proportions from adjacent medial occipitoparietal areas, from the superior temporal motion-sensitive complex centered on the middle temporal area (MT), and from ventral stream-associated areas. Feedback from the posterior parietal cortex and other association areas accounts for <10% of the connections. These results do not support the hypothesis that DM is specifically associated with a medial subcircuit of the dorsal stream, important for visuomotor integration. Instead, they suggest an early-stage visual-processing node capable of contributing across cortical streams, much as V1 and V2 do. Thus, although DM may be important for providing visual inputs for guided body movements (which often depend on information contained in peripheral vision), this area is also likely to participate in other functions that require integration across wide expanses of visual space, such as perception of self-motion and contour completion.

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.

Thalamic afferents emphasize the different functions of macaque precuneate areas.

We studied the thalamic afferents to cortical areas in the precuneus using injections of retrograde fluorescent neuronal tracers in four male macaques (Macaca fascicularis). Six injections were within the limits of cytoarchitectural area PGm, one in area 31 and one in area PEci. Precuneate areas shared strong input from the posterior thalamus (lateral posterior nucleus and pulvinar complex) and moderate input from the medial, lateral, and intralaminar thalamic regions. Area PGm received strong connections from the subdivisions of the pulvinar linked to association and visual function (the medial and lateral nuclei), whereas areas 31 and PEci received afferents from the oral division of the pulvinar. All three cytoarchitectural areas also received input from subdivisions of the lateral thalamus linked to motor function (ventral lateral and ventral anterior nuclei), with area PEci receiving additional input from a subdivision linked to somatosensory function (ventral posterior lateral nucleus). Finally, only PGm received substantial limbic association afferents, mainly via the lateral dorsal nucleus. These results indicate that area PGm integrates information from visual association, motor and limbic regions of the thalamus, in line with a hypothesized role in spatial cognition, including navigation. By comparison, dorsal precuneate areas (31 and PEci) are more involved in sensorimotor functions, being akin to adjacent areas of the dorsal parietal cortex.

Neurons Modulated by Action Execution and Observation in the Macaque Medial Parietal Cortex.

The observation of an action evokes discharges in a rich network of cortical areas [1-14]. In the present study, we have evaluated the effect of grasp execution and of the observation of others' grasping on the activity of neurons in the medial parietal area V6A, an area of the reach-to-grasp network never explored to date in this regard. Although V6A neurons are typically active during one's own grasping execution but not while one observes another's grasping, a minority of neurons showed mirror properties, active both when monkeys performed the task and when they observed it being performed by the experimenter. Recent studies have shown that the discharge of mirror neurons may vary from congruent to noncongruent [7, 10, 15-17], but most mirror neurons show a clear relation between the visual action they respond to and the motor response they code [10], thus matching the sensory description of an observed action with its corresponding internal motor representation. In all V6A putative mirror neurons, instead, neural representations during execution and observation were highly dissimilar, discounting the possibility that V6A specifically encodes the grip type performed by another agent. Notably, we have found that in these neurons, the neural representation of an object changed according to whether grasping was allowed or performed and whether the object was the target of another agent's grasping. In other words, rather than code another agent's observed action, V6A neurons appear to primarily encode the relevance, in the grasping context, of the target object.

Anatomical and physiological definition of the motor cortex of the marmoset monkey.

We used a combination of anatomical and physiological techniques to define the primary motor cortex (M1) of the marmoset monkey and its relationship to adjacent cortical fields. Area M1, defined as a region containing a representation of the entire body and showing the highest excitability to intracortical microstimulation, is architecturally heterogeneous: it encompasses both the caudal part of the densely myelinated "gigantopyramidal" cortex (field 4) and a lateral region, corresponding to the face representation, which is less myelinated and has smaller layer 5 pyramidal cells (field 4c). Rostral to M1 is a field that is strongly reminiscent of field 4 in terms of cyto- and myeloarchitecture but that in the marmoset is poorly responsive to microstimulation. Anatomical tracing experiments revealed that this rostral field is interconnected with visual areas of the posterior parietal cortex, whereas M1 itself has no such connections. For these reasons, we considered this field to be best described as part of the dorsal premotor cortex and adopted the designation 6Dc. Histological criteria were used to define other fields adjacent to M1, including medial and ventral subdivisions of the premotor cortex (fields 6M and 6V) and the rostral somatosensory field (area 3a), as well as a rostral subdivision of the dorsal premotor area (field 6Dr). These results suggest a basic plan underlying the histological organization of the caudal frontal cortex in different simian species, which has been elaborated during the evolution of larger species of primate by creation of further morphological and functional subdivisions.