Area AIP Research Articles

Information-processing dynamics in neural networks of macaque cerebral cortex reflect cognitive state and behavior

One of the essential functions of biological neural networks is the processing of information. This includes everything from processing sensory information to perceive the environment, up to processing motor information to interact with the environment. Due to methodological limitations, it has been historically unclear how information processing changes during different cognitive or behavioral states and to what extent information is processed within or between the network of neurons in different brain areas. In this study, we leverage recent advances in the calculation of information dynamics to explore neural-level processing within and between the frontoparietal areas AIP, F5, and M1 during a delayed grasping task performed by three macaque monkeys. While information processing was high within all areas during all cognitive and behavioral states of the task, interareal processing varied widely: During visuomotor transformation, AIP and F5 formed a reciprocally connected processing unit, while no processing was present between areas during the memory period. Movement execution was processed globally across all areas with predominance of processing in the feedback direction. Furthermore, the fine-scale network structure reconfigured at the neuron level in response to different grasping conditions, despite no differences in the overall amount of information present. These results suggest that areas dynamically form higher-order processing units according to the cognitive or behavioral demand and that the information-processing network is hierarchically organized at the neuron level, with the coarse network structure determining the behavioral state and finer changes reflecting different conditions.

Complementary contribution of the medial and lateral human parietal cortex to grasping: a repetitive TMS study.

The dexterous control of our grasping actions relies on the cooperative activation of many brain areas. In the parietal lobe, 2 grasp-related areas collaborate to orchestrate an accurate grasping action: dorsolateral area AIP and dorsomedial area V6A. Single-cell recordings in monkeys and fMRI studies in humans have suggested that both these areas specify grip aperture and wrist orientation, but encode these grasping parameters differently, depending on the context. To elucidate the causal role of phAIP and hV6A, we stimulated these areas, while participants were performing grasping actions (unperturbed grasping). rTMS over phAIP impaired the wrist orientation process, whereas stimulation over hV6A impaired grip aperture encoding. In a small percentage of trials, an unexpected reprogramming of grip aperture or wrist orientation was required (perturbed grasping). In these cases, rTMS over hV6A or over phAIP impaired reprogramming of both grip aperture and wrist orientation. These results represent the first direct demonstration of a different encoding of grasping parameters by 2 grasp-related parietal areas.

The human posterior parietal cortex: effective connectome, and its relation to function.

The effective connectivity between 21 regions in the human posterior parietal cortex, and 360 cortical regions was measured in 171 Human Connectome Project (HCP) participants using the HCP atlas, and complemented with functional connectivity and diffusion tractography. Intraparietal areas LIP, VIP, MIP, and AIP have connectivity from early cortical visual regions, and to visuomotor regions such as the frontal eye fields, consistent with functions in eye saccades and tracking. Five superior parietal area 7 regions receive from similar areas and from the intraparietal areas, but also receive somatosensory inputs and connect with premotor areas including area 6, consistent with functions in performing actions to reach for, grasp, and manipulate objects. In the anterior inferior parietal cortex, PFop, PFt, and PFcm are mainly somatosensory, and PF in addition receives visuo-motor and visual object information, and is implicated in multimodal shape and body image representations. In the posterior inferior parietal cortex, PFm and PGs combine visuo-motor, visual object, and reward input and connect with the hippocampal system. PGi in addition provides a route to motion-related superior temporal sulcus regions involved in social interactions. PGp has connectivity with intraparietal regions involved in coordinate transforms and may be involved in idiothetic update of hippocampal visual scene representations.

Local and system mechanisms for action execution and observation in parietal and premotor cortices

SummaryThe action observation network (AON) includes a system of brain areas largely shared with action execution in both human and nonhuman primates. Yet temporal and tuning specificities of distinct areas and of physiologically identified neuronal classes in the encoding of self and others’ action remain unknown. We recorded the activity of 355 single units from three crucial nodes of the AON, the anterior intraparietal area (AIP), and premotor areas F5 and F6, while monkeys performed a Go/No-Go grasping task and observed an experimenter performing it. At the system level, during task execution, F6 displays a prevalence of suppressed neurons and signals whether an action has to be performed, whereas AIP and F5 share a prevalence of facilitated neurons and remarkable target selectivity; during task observation, F5 stands out for its unique prevalence of facilitated neurons and its stronger and earlier modulation than AIP and F6. By applying unsupervised clustering of spike waveforms, we found distinct cell classes unevenly distributed across areas, with different firing properties and carrying specific visuomotor signals. Broadly spiking neurons exhibited a balanced amount of facilitated and suppressed activity during action execution and observation, whereas narrower spiking neurons showed more mutually facilitated responses during the execution of one’s own and others’ action, particularly in areas AIP and F5. Our findings elucidate the time course of activity and firing properties of neurons in the AON during one’s own and others’ action, from the system level of anatomically distinct areas to the local level of physiologically distinct cell classes.

Thalamic Inputs to Posterior Parietal Cortical Areas Involved in Skilled Forelimb Movement and Tool Use in the Capuchin Monkey.

The posterior parietal cortex (PPC) is a central hub for the primate forebrain networks that control skilled manual behavior, including tool use. Here, we quantified and compared the sources of thalamic input to electrophysiologically-identified hand/forearm-related regions of several PPC areas, namely areas 5v, AIP, PFG, and PF, of the capuchin monkey (Sapajus sp). We found that these areas receive most of their thalamic connections from the Anterior Pulvinar (PuA), Lateral Posterior (LP) and Medial Pulvinar (PuM) nuclei. Each PPC area receives a specific combination of projections from these nuclei, and fewer additional projections from other nuclei. Moreover, retrograde labeling of the cells innervating different PPC areas revealed substantial intermingling of these cells within the thalamus. Differences in thalamic input may contribute to the different functional properties displayed by the PPC areas. Furthermore, the observed innervation of functionally-related PPC domains from partly intermingled thalamic cell populations accords with the notion that higher-order thalamic inputs may dynamically regulate functional connectivity between cortical areas.

Neural coding of intended and executed grasp force in macaque areas AIP, F5, and M1

Considerable progress has been made over the last decades in characterizing the neural coding of hand shape, but grasp force has been largely ignored. We trained two macaque monkeys (Macaca mulatta) on a delayed grasping task where grip type and grip force were instructed. Neural population activity was recorded from areas relevant for grasp planning and execution: the anterior intraparietal area (AIP), F5 of the ventral premotor cortex, and the hand area of the primary motor cortex (M1). Grasp force was strongly encoded by neural populations of all three areas, thereby demonstrating for the first time the coding of grasp force in single- and multi-units of AIP. Neural coding of intended grasp force was most strongly represented in area F5. In addition to tuning analysis, a dimensionality reduction method revealed low-dimensional responses to grip type and grip force. Additionally, this method revealed a high correlation between latent variables of the neural population representing grasp force and the corresponding latent variables of electromyographic forearm muscle activity. Our results therefore suggest an important role of the cortical areas AIP, F5, and M1 in coding grasp force during movement execution as well as of F5 for coding intended grasp force.

Axonal Projections From the Middle Temporal Area in the Common Marmoset.

Neural activity in the middle temporal (MT) area is modulated by the direction and speed of motion of visual stimuli. The area is buried in a sulcus in the macaque, but exposed to the cortical surface in the marmoset, making the marmoset an ideal animal model for studying MT function. To better understand the details of the roles of this area in cognition, underlying anatomical connections need to be clarified. Because most anatomical tracing studies in marmosets have used retrograde tracers, the axonal projections remain uncharacterized. In order to examine axonal projections from MT, we utilized adeno-associated viral (AAV) tracers, which work as anterograde tracers by expressing either green or red fluorescent protein in infected neurons. AAV tracers were injected into three sites in MT based on retinotopy maps obtained via in vivo optical intrinsic signal imaging. Brains were sectioned and divided into three series, one for fluorescent image scanning and two for myelin and Nissl substance staining to identify specific brain areas. Overall projection patterns were similar across the injections. MT projected to occipital visual areas V1, V2, V3 (VLP) and V4 (VLA) and surrounding areas in the temporal cortex including MTC (V4T), MST, FST, FSTv (PGa/IPa) and TE3. There were also projections to the dorsal visual pathway, V3A (DA), V6 (DM) and V6A, the intraparietal areas AIP, LIP, MIP, frontal A4ab and the prefrontal cortex, A8aV and A8C. There was a visuotopic relationship with occipital visual areas. In a marmoset in which two tracer injections were made, the projection targets did not overlap in A8aV and AIP, suggesting topographic projections from different parts of MT. Most of these areas are known to send projections back to MT, suggesting that they are reciprocally connected with it.

Cortical Afferents and Myeloarchitecture Distinguish the Medial Intraparietal Area (MIP) from Neighboring Subdivisions of the Macaque Cortex.

The parietal reach region (PRR) in the medial bank of the macaque intraparietal sulcus has been a subject of considerable interest in research aimed at the development of brain-controlled prosthetic arms, but its anatomical organization remains poorly characterized. We examined the anatomical organization of the putative PRR territory based on myeloarchitecture and retrograde tracer injections. We found that the medial bank includes three areas: an extension of the dorsal subdivision of V6A (V6Ad), the medial intraparietal area (MIP), and a subdivision of area PE (PEip). Analysis of corticocortical connections revealed that both V6Ad and MIP receive inputs from visual area V6; the ventral subdivision of V6A (V6Av); medial (PGm, 31), superior (PEc), and inferior (PFG/PF) parietal association areas; and intraparietal areas AIP and VIP. They also receive long-range projections from the superior temporal sulcus (MST, TPO), cingulate area 23, and the dorsocaudal (area F2) and ventral (areas F4/F5) premotor areas. In comparison with V6Ad, MIP receives denser input from somatosensory areas, the primary motor cortex, and the medial motor fields, as well as from visual cortex in the ventral precuneate cortex and frontal regions associated with oculomotor guidance. Unlike MIP, V6Ad receives stronger visual input, from the caudal inferior parietal cortex (PG/Opt) and V6Av, whereas PEip shows marked emphasis on anterior parietal, primary motor, and ventral premotor connections. These anatomical results suggest that MIP and V6A have complementary roles in sensorimotor behavior, with MIP more directly involved in movement planning and execution in comparison with V6A.

Mapping the complex topological organization of the human parietal face area

The macaque monkey ventral intraparietal area (VIP) contains neurons with aligned visual-tactile receptive fields anchored to the face and upper body. Our previous fMRI studies using standard head coils found a human parietal face area (VIP+ complex; putative macaque VIP homologue) containing superimposed topological maps of the face and near-face visual space. Here, we construct high signal-to-noise surface coils and used phase-encoded air puffs and looming stimuli to map topological organization of the parietal face area at higher resolution. This area is consistently identified as a region extending between the superior postcentral sulcus and the upper bank of the anterior intraparietal sulcus (IPS), avoiding the fundus of IPS. Using smaller voxel sizes, our surface coils picked up strong fMRI signals in response to tactile and visual stimuli. By analyzing tactile and visual maps in our current and previous studies, we constructed a set of topological models illustrating commonalities and differences in map organization across subjects. The most consistent topological feature of the VIP+ complex is a central-anterior upper face (and upper visual field) representation adjoined by lower face (and lower visual field) representations ventrally (laterally) and/or dorsally (medially), potentially forming two subdivisions VIPv (ventral) and VIPd (dorsal). The lower visual field representations typically extend laterally into the anterior IPS to adjoin human area AIP, and medially to overlap with the parietal body areas at the superior parietal ridge. Significant individual variations are then illustrated to provide an accurate and comprehensive view of the topological organization of the parietal face area.

The extended object-grasping network.

Grasping is the most important skilled motor act of primates. It is based on a series of sensorimotor transformations through which the affordances of the objects to be grasped are transformed into appropriate hand movements. It is generally accepted that a circuit formed by inferior parietal areas AIP and PFG and ventral premotor area F5 represents the core circuit for sensorimotor transformations for grasping. However, selection and control of appropriate grip should also depend on higher-order information, such as the meaning of the object to be grasped, and the overarching goal of the action in which grasping is embedded. In this review, we describe recent findings showing that specific sectors of the ventrolateral prefrontal cortex are instrumental in controlling higher-order aspects of grasping. We show that these prefrontal sectors control the premotor cortex through two main gateways: the anterior subdivision of ventral area F5-sub-area F5a-, and the pre-supplementary area (area F6). We then review functional studies showing that both F5a and F6, besides being relay stations of prefrontal information, also play specific roles in grasping. Namely, sub-area F5a is involved in stereoscopic analysis of 3D objects, and in planning cue-dependent grasping activity. As for area F6, this area appears to play a crucial role in determining when to execute the motor program encoded in the parieto-premotor circuit. The recent discovery that area F6 contains a set of neurons encoding specific grip types suggests that this area, besides controlling "when to go", also may control the grip type, i.e., "how to go". We conclude by discussing clinical syndromes affecting grasping actions and their possible mechanisms.

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.

Object vision to hand action in macaque parietal, premotor, and motor cortices.

Grasping requires translating object geometries into appropriate hand shapes. How the brain computes these transformations is currently unclear. We investigated three key areas of the macaque cortical grasping circuit with microelectrode arrays and found cooperative but anatomically separated visual and motor processes. The parietal area AIP operated primarily in a visual mode. Its neuronal population revealed a specialization for shape processing, even for abstract geometries, and processed object features ultimately important for grasping. Premotor area F5 acted as a hub that shared the visual coding of AIP only temporarily and switched to highly dominant motor signals towards movement planning and execution. We visualize these non-discrete premotor signals that drive the primary motor cortex M1 to reflect the movement of the grasping hand. Our results reveal visual and motor features encoded in the grasping circuit and their communication to achieve transformation for grasping.

Representation of continuous hand and arm movements in macaque areas M1, F5, and AIP: a comparative decoding study

Objective. In the last decade, multiple brain areas have been investigated with respect to their decoding capability of continuous arm or hand movements. So far, these studies have mainly focused on motor or premotor areas like M1 and F5. However, there is accumulating evidence that anterior intraparietal area (AIP) in the parietal cortex also contains information about continuous movement. Approach. In this study, we decoded 27 degrees of freedom representing complete hand and arm kinematics during a delayed grasping task from simultaneously recorded activity in areas M1, F5, and AIP of two macaque monkeys (Macaca mulatta). Main results. We found that all three areas provided decoding performances that lay significantly above chance. In particular, M1 yielded highest decoding accuracy followed by F5 and AIP. Furthermore, we provide support for the notion that AIP does not only code categorical visual features of objects to be grasped, but also contains a substantial amount of temporal kinematic information. Significance. This fact could be utilized in future developments of neural interfaces restoring hand and arm movements.

Shape representations in the primate dorsal visual stream

The primate visual system extracts object shape information for object recognition in the ventral visual stream. Recent research has demonstrated that object shape is also processed in the dorsal visual stream, which is specialized for spatial vision and the planning of actions. A number of studies have investigated the coding of 2D shape in the anterior intraparietal area (AIP), one of the end-stage areas of the dorsal stream which has been implicated in the extraction of affordances for the purpose of grasping. These findings challenge the current understanding of area AIP as a critical stage in the dorsal stream for the extraction of object affordances. The representation of three-dimensional (3D) shape has been studied in two interconnected areas known to be critical for object grasping: area AIP and area F5a in the ventral premotor cortex (PMv), to which AIP projects. In both areas neurons respond selectively to 3D shape defined by binocular disparity, but the latency of the neural selectivity is approximately 10 ms longer in F5a compared to AIP, consistent with its higher position in the hierarchy of cortical areas. Furthermore, F5a neurons were more sensitive to small amplitudes of 3D curvature and could detect subtle differences in 3D structure more reliably than AIP neurons. In both areas, 3D-shape selective neurons were co-localized with neurons showing motor-related activity during object grasping in the dark, indicating a close convergence of visual and motor information on the same clusters of neurons.

Exploring manual asymmetries during grasping: a dynamic causal modeling approach.

Recording of neural activity during grasping actions in macaques showed that grasp-related sensorimotor transformations are accomplished in a circuit constituted by the anterior part of the intraparietal sulcus (AIP), the ventral (F5) and the dorsal (F2) region of the premotor area. In humans, neuroimaging studies have revealed the existence of a similar circuit, involving the putative homolog of macaque areas AIP, F5, and F2. These studies have mainly considered grasping movements performed with the right dominant hand and only a few studies have measured brain activity associated with a movement performed with the left non-dominant hand. As a consequence of this gap, how the brain controls for grasping movement performed with the dominant and the non-dominant hand still represents an open question. A functional magnetic resonance imaging (fMRI) experiment has been conducted, and effective connectivity (dynamic causal modeling, DCM) was used to assess how connectivity among grasping-related areas is modulated by hand (i.e., left and right) during the execution of grasping movements toward a small object requiring precision grasping. Results underlined boosted inter-hemispheric couplings between dorsal premotor cortices during the execution of movements performed with the left rather than the right dominant hand. More specifically, they suggest that the dorsal premotor cortices may play a fundamental role in monitoring the configuration of fingers when grasping movements are performed by either the right and the left hand. This role becomes particularly evident when the hand less-skilled (i.e., the left hand) to perform such action is utilized. The results are discussed in light of recent theories put forward to explain how parieto-frontal connectivity is modulated by the execution of prehensile movements.

Co-Registering Kinematics and Evoked Related Potentials during Visually Guided Reach-to-Grasp Movements

BackgroundIn non-human primates grasp-related sensorimotor transformations are accomplished in a circuit involving the anterior intraparietal sulcus (area AIP) and both the ventral and the dorsal sectors of the premotor cortex (vPMC and dPMC, respectively). Although a human homologue of such a circuit has been identified, the time course of activation of these cortical areas and how such activity relates to specific kinematic events has yet to be investigated.Methodology/Principal FindingsWe combined kinematic and event-related potential techniques to explicitly test how activity within human grasping-related brain areas is modulated in time. Subjects were requested to reach towards and grasp either a small stimulus using a precision grip (i.e., the opposition of index finger and thumb) or a large stimulus using a whole hand grasp (i.e., the flexion of all digits around the stimulus). Results revealed a time course of activation starting at the level of parietal regions and continuing at the level of premotor regions. More specifically, we show that activity within these regions was tuned for specific grasps well before movement onset and this early tuning was carried over - as evidenced by kinematic analysis - during the preshaping period of the task.Conclusions/SignificanceData are discussed in terms of recent findings showing a marked differentiation across different grasps during premovement phases which was carried over into subsequent movement phases. These findings offer a substantial contribution to the current debate about the nature of the sensorimotor transformations underlying grasping. And provide new insights into the detailed movement information contained in the human preparatory activity for specific hand movements.

Three-dimensional Shape Coding in Grasping Circuits: A Comparison between the Anterior Intraparietal Area and Ventral Premotor Area F5a

Depth information is necessary for adjusting the hand to the three-dimensional (3-D) shape of an object to grasp it. The transformation of visual information into appropriate distal motor commands is critically dependent on the anterior intraparietal area (AIP) and the ventral premotor cortex (area F5), particularly the F5p sector. Recent studies have demonstrated that both AIP and the F5a sector of the ventral premotor cortex contain neurons that respond selectively to disparity-defined 3-D shape. To investigate the neural coding of 3-D shape and the behavioral role of 3-D shape-selective neurons in these two areas, we recorded single-cell activity in AIP and F5a during passive fixation of curved surfaces and during grasping of real-world objects. Similar to those in AIP, F5a neurons were either first- or second-order disparity selective, frequently showed selectivity for discrete approximations of smoothly curved surfaces that contained disparity discontinuities, and exhibited mostly monotonic tuning for the degree of disparity variation. Furthermore, in both areas, 3-D shape-selective neurons were colocalized with neurons that were active during grasping of real-world objects. Thus, area AIP and F5a contain highly similar representations of 3-D shape, which is consistent with the proposed transfer of object information from AIP to the motor system through the ventral premotor cortex.

Connectional Heterogeneity of the Ventral Part of the Macaque Area 46

We found that the ventral part of the prefrontal area 46 (46v) is connectionally heterogeneous. Specifically, the rostral part (46vr) displayed an almost exclusive and extensive intraprefrontal connectivity and extraprefrontal connections limited to area 24 and inferotemporal areas. In contrast, the caudal part (46vc) mostly displayed intraprefrontal connectivity with ventrolateral areas and robust connectivity with frontal and parietal sensorimotor areas. Based on a topographic organization of these connections, 3 fields were identified in area 46vc. A caudal field (caudal 46vc) was preferentially connected to oculomotor prearcuate (8/FEF, 45B, and 8r) and inferior parietal areas. The other 2, located more rostrally, in the bank of the principal sulcus (rostral 46vc/bank) and on the ventrolateral convexity cortex (rostral 46vc/convexity), respectively, were connected with hand/mouth-related (F5a, 44) ventral premotor areas, area SII, and the insula. However, rostral 46vc/convexity was also connected to the hand-related area AIP, whereas rostral 46vc/bank to hand/arm-related areas PFG and PG, to PGop, and to areas 11 and 24. The present data suggest a differential role in executive functions of areas 46vr and 46vc and a differential involvement of different parts of area 46vc in higher level integration for oculomotor behavior and goal-directed arm, hand, and mouth actions.

Object or grip type representation? A comparative population study of macaque hand grasping areas M1, F5, and AIP

Object or grip type representation? A comparative population study of macaque hand grasping areas M1, F5, and AIP

Disparity Context Processing in the Primate Brain: And If the Question was Both ?What? and ?When??

Disparity Context Processing in the Primate Brain: And If the Question was Both ?What? and ?When??