Simona Monaco

Functional Magnetic Resonance Imaging Reveals the Neural Substrates of Arm Transport and Grip Formation in Reach-to-Grasp Actions in Humans

Picking up a cup requires transporting the arm to the cup (transport component) and preshaping the hand appropriately to grasp the handle (grip component). Here, we used functional magnetic resonance imaging to examine the human neural substrates of the transport component and its relationship with the grip component. Participants were shown three-dimensional objects placed either at a near location, adjacent to the hand, or at a far location, within reach but not adjacent to the hand. Participants performed three tasks at each location as follows: (1) touching the object with the knuckles of the right hand; (2) grasping the object with the right hand; or (3) passively viewing the object. The transport component was manipulated by positioning the object in the far versus the near location. The grip component was manipulated by asking participants to grasp the object versus touching it. For the first time, we have identified the neural substrates of the transport component, which include the superior parieto-occipital cortex and the rostral superior parietal lobule. Consistent with past studies, we found specialization for the grip component in bilateral anterior intraparietal sulcus and left ventral premotor cortex; now, however, we also find activity for the grasp even when no transport is involved. In addition to finding areas specialized for the transport and grip components in parietal cortex, we found an integration of the two components in dorsal premotor cortex and supplementary motor areas, two regions that may be important for the coordination of reach and grasp.

Functional magnetic resonance adaptation reveals the involvement of the dorsomedial stream in hand orientation for grasping

Reach-to-grasp actions require coordination of different segments of the upper limbs. Previous studies have examined the neural substrates of arm transport and hand grip components of such actions; however, a third component has been largely neglected: the orientation of the wrist and hand appropriately for the object. Here we used functional magnetic resonance imaging adaptation (fMRA) to investigate human brain areas involved in processing hand orientation during grasping movements. Participants used the dominant right hand to grasp a rod with the four fingers opposing the thumb or to reach and touch the rod with the knuckles without visual feedback. In a control condition, participants passively viewed the rod. Trials in a slow event-related design consisted of two sequential stimuli in which the rod orientation changed (requiring a change in wrist posture while grasping but not reaching or looking) or remained the same. We found reduced activation, that is, adaptation, in superior parieto-occipital cortex (SPOC) when the object was repeatedly grasped with the same orientation. In contrast, there was no adaptation when reaching or looking at an object in the same orientation, suggesting that hand orientation, rather than object orientation, was the critical factor. These results agree with recent neurophysiological research showing that a parieto-occipital area of macaque (V6A) is modulated by hand orientation during reach-to-grasp movements. We suggest that the human dorsomedial stream, like that in the macaque, plays a key role in processing hand orientation in reach-to-grasp movements.

Human fMRI Reveals That Delayed Action Re-Recruits Visual Perception

Behavioral and neuropsychological research suggests that delayed actions rely on different neural substrates than immediate actions; however, the specific brain areas implicated in the two types of actions remain unknown. We used functional magnetic resonance imaging (fMRI) to measure human brain activation during delayed grasping and reaching. Specifically, we examined activation during visual stimulation and action execution separated by a 18-s delay interval in which subjects had to remember an intended action toward the remembered object. The long delay interval enabled us to unambiguously distinguish visual, memory-related, and action responses. Most strikingly, we observed reactivation of the lateral occipital complex (LOC), a ventral-stream area implicated in visual object recognition, and early visual cortex (EVC) at the time of action. Importantly this reactivation was observed even though participants remained in complete darkness with no visual stimulation at the time of the action. Moreover, within EVC, higher activation was observed for grasping than reaching during both vision and action execution. Areas in the dorsal visual stream were activated during action execution as expected and, for some, also during vision. Several areas, including the anterior intraparietal sulcus (aIPS), dorsal premotor cortex (PMd), primary motor cortex (M1) and the supplementary motor area (SMA), showed sustained activation during the delay phase. We propose that during delayed actions, dorsal-stream areas plan and maintain coarse action goals; however, at the time of execution, motor programming requires re-recruitment of detailed visual information about the object through reactivation of (1) ventral-stream areas involved in object perception and (2) early visual areas that contain richly detailed visual representations, particularly for grasping.

Functional Magnetic Resonance Imaging Adaptation Reveals the Cortical Networks for Processing Grasp-Relevant Object Properties

Grasping behaviors require the selection of grasp-relevant object dimensions, independent of overall object size. Previous neuroimaging studies found that the intraparietal cortex processes object size, but it is unknown whether the graspable dimension (i.e., grasp axis between selected points on the object) or the overall size of objects triggers activation in that region. We used functional magnetic resonance imaging adaptation to investigate human brain areas involved in processing the grasp-relevant dimension of real 3-dimensional objects in grasping and viewing tasks. Trials consisted of 2 sequential stimuli in which the objects grasp-relevant dimension, its global size, or both were novel or repeated. We found that calcarine and extrastriate visual areas adapted to object size regardless of the grasp-relevant dimension during viewing tasks. In contrast, the superior parietal occipital cortex (SPOC) and lateral occipital complex of the left hemisphere adapted to the grasp-relevant dimension regardless of object size and task. Finally, the dorsal premotor cortex adapted to the grasp-relevant dimension in grasping, but not in viewing, tasks, suggesting that motor processing was complete at this stage. Taken together, our results provide a complete cortical circuit for progressive transformation of general object properties into grasp-related responses.

Contribution of visual and proprioceptive information to the precision of reaching movements

Ren et al. (J Neurophysiol 96:1464–1477, 2006) found that saccades to visual targets became less accurate when somatosensory information about hand location was added, suggesting that saccades rely mainly on vision. We conducted two kinematic experiments to examine whether or not reaching movements would also show such strong reliance on vision. In Experiment 1, subjects used their dominant right hand to perform reaches, with or without a delay, to an external visual target or to their own left fingertip positioned either by the experimenter or by the participant. Unlike saccades, reaches became more accurate and precise when proprioceptive information was available. In Experiment 2, subjects reached toward external or bodily targets with differing amounts of visual information. Proprioception improved performance only when vision was limited. These results indicate that the reaching system has a better internal model for limb positions than does the saccade system.

Neural correlates of object size and object location during grasping actions

The visuo‐motor channel hypothesis (Jeannerod, 1981) postulates that grasping movements consist of a grip and a transport component differing in their reliance on intrinsic vs. extrinsic object properties (e.g. size vs. location, respectively). While recent neuroimaging studies have revealed separate brain areas implicated in grip and transport components within the parietal lobe, less is known about the neural processing of extrinsic and intrinsic properties of objects for grasping actions. We used functional magnetic resonance imaging adaptation to examine the cortical areas involved in processing object size, object location or both. Participants grasped (using the dominant right hand) or passively viewed sequential pairs of objects that could differ in size, location or both. We hypothesized that if intrinsic and extrinsic object properties are processed separately, as suggested by the visuo‐motor channel hypothesis, we would observe adaptation to object size in areas that code the grip and adaptation to location in areas that code the transport component. On the other hand, if intrinsic and extrinsic object properties are not processed separately, brain areas involved in grasping may show adaptation to both object size and location. We found adaptation to object size for grasping movements in the left anterior intraparietal sulcus (aIPS), in agreement with the idea that object size is processed separately from location. In addition, the left superior parietal occipital sulcus (SPOC), primary somatosensory and motor area (S1/M1), precuneus, dorsal premotor cortex (PMd), and supplementary motor area (SMA) showed non‐additive adaptation to both object size and location. We propose different roles for the aIPS as compared with the SPOC, S1/M1, precuneus, PMd and SMA. In particular, while the aIPS codes intrinsic object properties, which are relevant for hand preshaping and force scaling, area SPOC, S1/M1, precuneus, PMd and SMA code intrinsic as well as extrinsic object properties, both of which are relevant for digit positioning during grasping.

Allocentric versus Egocentric Representation of Remembered Reach Targets in Human Cortex

The location of a remembered reach target can be encoded in egocentric and/or allocentric reference frames. Cortical mechanisms for egocentric reach are relatively well described, but the corresponding allocentric representations are essentially unknown. Here, we used an event-related fMRI design to distinguish human brain areas involved in these two types of representation. Our paradigm consisted of three tasks with identical stimulus display but different instructions: egocentric reach (remember absolute target location), allocentric reach (remember target location relative to a visual landmark), and a nonspatial control, color report (report color of target). During the delay phase (when only target location was specified), the egocentric and allocentric tasks elicited widely overlapping regions of cortical activity (relative to the control), but with higher activation in parietofrontal cortex for egocentric task and higher activation in early visual cortex for allocentric tasks. In addition, egocentric directional selectivity (target relative to gaze) was observed in the superior occipital gyrus and the inferior occipital gyrus, whereas allocentric directional selectivity (target relative to a visual landmark) was observed in the inferior temporal gyrus and inferior occipital gyrus. During the response phase (after movement direction had been specified either by reappearance of the visual landmark or a pro-/anti-reach instruction), the parietofrontal network resumed egocentric directional selectivity, showing higher activation for contralateral than ipsilateral reaches. These results show that allocentric and egocentric reach mechanisms use partially overlapping but different cortical substrates and that directional specification is different for target memory versus reach response.

Integration of visual and auditory information for hand actions: preliminary evidence for the contribution of natural sounds to grasping

When we reach out to grasp objects, vision plays a major role in the control of our movements. Nevertheless, other sensory modalities contribute to the fine-tuning of our actions. Even olfaction has been shown to play a role in the scaling of movements directed at objects. Much less is known about how auditory information might be used to program grasping movements. The aim of our study was to investigate how the sound of a target object affects the planning of grasping movements in normal right-handed subjects. We performed an experiment in which auditory information could be used to infer size of targets when the availability of visual information was varied from trial to trial. Classical kinematic parameters (such as grip aperture) were measured to evaluate the influence of auditory information. In addition, an optimal inference modeling was applied to the data. The scaling of grip aperture indicated that the introduction of sound allowed subjects to infer the size of the object when vision was not available. Moreover, auditory information affected grip aperture even when vision was available. Our findings suggest that the differences in the natural impact sounds of objects of different sizes being placed on a surface can be used to plan grasping movements.

Flexible Reference Frames for Grasp Planning in Human Parietofrontal Cortex

Abstract Reaching to a location in space is supported by a cortical network that operates in a variety of reference frames. Computational models and recent fMRI evidence suggest that this diversity originates from neuronal populations dynamically shifting between reference frames as a function of task demands and sensory modality. In this human fMRI study, we extend this framework to nonmanipulative grasping movements, an action that depends on multiple properties of a target, not only its spatial location. By presenting targets visually or somaesthetically, and by manipulating gaze direction, we investigate how information about a target is encoded in gaze- and body-centered reference frames in dorsomedial and dorsolateral grasping-related circuits. Data were analyzed using a novel multivariate approach that combines classification and cross-classification measures to explicitly aggregate evidence in favor of and against the presence of gaze- and body-centered reference frames. We used this approach to determine whether reference frames are differentially recruited depending on the availability of sensory information, and where in the cortical networks there is common coding across modalities. Only in the left anterior intraparietal sulcus (aIPS) was coding of the grasping target modality dependent: predominantly gaze-centered for visual targets and body-centered for somaesthetic targets. Left superior parieto-occipital cortex consistently coded targets for grasping in a gaze-centered reference frame. Left anterior precuneus and premotor areas operated in a modality-independent, body-centered frame. These findings reveal how dorsolateral grasping area aIPS could play a role in the transition between modality-independent gaze-centered spatial maps and body-centered motor areas.

Impaired peripheral reaching and on-line corrections in patient DF: Optic ataxia with visual form agnosia

An influential model of vision suggests the presence of two visual streams within the brain: a dorsal occipito-parietal stream which mediates action and a ventral occipito-temporal stream which mediates perception. One of the cornerstones of this model is DF, a patient with visual form agnosia following bilateral ventral stream lesions. Despite her inability to identify and distinguish visual stimuli, DF can still use visual information to control her hand actions towards these stimuli. These observations have been widely interpreted as demonstrating a double dissociation from optic ataxia, a condition observed after bilateral dorsal stream damage in which patients are unable to act towards objects that they can recognize. In Experiment 1, we investigated how patient DF performed on the classical diagnostic task for optic ataxia, reaching in central and peripheral vision. We replicated recent findings that DF is remarkably inaccurate when reaching to peripheral targets, but not when reaching in free vision. In addition we present new evidence that her peripheral reaching errors follow the optic ataxia pattern increasing with target eccentricity and being biased towards fixation. In Experiments 2 and 3, for the first time we examined DFs on-line control of reaching using a double-step paradigm in fixation-controlled and free-vision versions of the task. DF was impaired when performing fast on-line corrections on all conditions tested, similarly to optic ataxia patients. Our findings question the long-standing assumption that DFs dorsal visual stream is functionally intact and that her on-line visuomotor control is spared. In contrast, in addition to visual form agnosia, DF also has visuomotor symptoms of optic ataxia which are most likely explained by bilateral damage to the superior parietal-occipital cortex (SPOC). We thus conclude that patient DF can no longer be considered as an appropriate single-case model for testing the neural basis of perception and action dissociations.