Eugene Tunik

Virtual lesions of the anterior intraparietal area disrupt goal-dependent on-line adjustments of grasp

Adaptive motor behavior requires efficient error detection and correction. The posterior parietal cortex is critical for on-line control of reach-to-grasp movements. Here we show a causal relationship between disruption of cortical activity within the anterior intraparietal sulcus (aIPS) by transcranial magnetic stimulation (TMS) and disruption of goal-directed prehensile actions (either grip size or forearm rotation, depending on the task goal, with reaching preserved in either case). Deficits were elicited by applying TMS within 65 ms after object perturbation, which attributes a rapid control process on the basis of visual feedback to aIPS. No aperture deficits were produced when TMS was applied to a more caudal region within the intraparietal sulcus, to the parieto-occipital complex (putative V6, V6A) or to the hand area of primary motor cortex. We contend that aIPS is critical for dynamic error detection during goal-dependent reach-to-grasp action that is visually guided.

Sensorimotor training in virtual reality: A review

Recent experimental evidence suggests that rapid advancement of virtual reality (VR) technologies has great potential for the development of novel strategies for sensorimotor training in neurorehabilitation. We discuss what the adaptive and engaging virtual environments can provide for massive and intensive sensorimotor stimulation needed to induce brain reorganization.Second, discrepancies between the veridical and virtual feedback can be introduced in VR to facilitate activation of targeted brain networks, which in turn can potentially speed up the recovery process. Here we review the existing experimental evidence regarding the beneficial effects of training in virtual environments on the recovery of function in the areas of gait,upper extremity function and balance, in various patient populations. We also discuss possible mechanisms underlying these effects. We feel that future research in the area of virtual rehabilitation should follow several important paths. Imaging studies to evaluate the effects of sensory manipulation on brain activation patterns and the effect of various training parameters on long term changes in brain function are needed to guide future clinical inquiry. Larger clinical studies are also needed to establish the efficacy of sensorimotor rehabilitation using VR in various clinical populations and most importantly, to identify VR training parameters that are associated with optimal transfer to real-world functional improvements.

Beyond grasping: Representation of action in human anterior intraparietal sulcus

The fronto-parietal network has been implicated in the processing of multisensory information for motor control. Recent methodological advances with both fMRI and TMS provide the opportunity to dissect the functionality of this extensive network in humans and may identify distinct contributions of local neural populations within this circuit that are not only related to motor planning, but to goal oriented behavior as a whole. Herein, we review and make parallels between experiments in monkeys and humans on a broad array of motor as well as non-motor tasks in order to characterize the specific contribution of a region in the parietal lobe, the anterior intraparietal sulcus (aIPS). The intent of this article is to review: (1) the historical perspectives on the parietal lobe, particularly the aIPS; (2) extend and update these perspectives based on recent empirical data; and (3) discuss the potential implications of the revised functionality of the aIPS in relationship to complex goal oriented behavior and social interaction. Our contention is that aIPS is a critical node within a network involved in the higher order dynamic control of action, including representation of intended action goals. These findings may be important not only for guiding the design of future experiments investigating related issues but may also have valuable utility in other fields, such social neuroscience and biomedical engineering.

The Anterior Intraparietal Sulcus Mediates Grasp Execution, Independent of Requirement to Update: New Insights from Transcranial Magnetic Stimulation

Although a role of the intraparietal sulcus (IPS) in grasping is becoming evident, the specific contribution of regions within the IPS remains undefined. In this vein, transcranial magnetic stimulation (TMS) was delivered to the anterior (aIPS), middle (mIPS), and caudal (cIPS) IPS in two tasks designed to dissociate the potential roles of the IPS in either grasp planning or execution (task 1) and its involvement in error detection or error correction (task 2). Determining the involvement of specific regions of the IPS in perceptual (planning and error detection) versus motor (execution and correction) components of grasping allowed us to assess the ecological validity of competing computational models attempting to simulate reach-to-grasp movements. In task 1, we demonstrate that, when no on-line adjustment is necessary, TMS to aIPS (but not mIPS or cIPS) disrupts grasping; this disruption is only elicited when TMS is applied during the execution (but not the planning) phase of the movement. Task 2 reveals that TMS to aIPS (but not mIPS or cIPS) disrupts grasping in the presence of a perturbation; this disruption is only elicited when TMS is applied during the error correction (but not error detection) phase of the movement. We propose that the specific contribution of the aIPS in grasping is in the on-line computation of a difference vector based on motor goal, efference copy, and sensory inputs. This computation is performed for both stable and perturbed motor goals.

Ventral and dorsal stream contributions to the online control of immediate and delayed grasping: A TMS approach

According to Milner and Goodales theory of the two visual streams, the dorsal (action) stream controls actions in real-time, whereas the ventral (perceptual) stream stores longer-term information for object identification. By this account, the dorsal stream subserves actions carried out immediately. However, when a delay is required before the response, the ventral (perceptual) stream is recruited. Indeed, a neuroimaging study from our lab has found reactivation of an area within the ventral stream, the lateral occipital (LO) cortex, at the time of action even when no visual stimulus was present. To tease apart the contribution of specific areas within the dorsal and ventral streams to the online control of grasping under immediate and delayed conditions, we used transcranial magnetic stimulation (TMS) to the anterior intraparietal sulcus (aIPS) and to LO. We show that while TMS to aIPS affected grasp under both immediate and delayed conditions, TMS to LO influenced grasp only under delayed movement conditions. The effects of TMS were restricted to early movement kinematics (i.e. within 300 ms) due to the transient nature of TMS, which was always delivered simultaneous with movement onset. We discuss the implications of our findings in relation to interactions between the dorsal and ventral streams.

Hand preshaping in Parkinson’s disease: effects of visual feedback and medication state

Previous studies in our laboratory examining pointing and reach-to-grasp movements of Parkinson’s disease patients (PDPs) have found that PDPs exhibit specific deficits in movement coordination and in the sensorimotor transformations required to accurately guide movements. We have identified a particular difficulty in matching unseen limb position, sensed by proprioception, with a visible target. In the present work, we further explored aspects of complex sensorimotor transformation and motor coordination using a reach-to-grasp task in which object shape, visual feedback, and dopaminergic medication were varied. Normal performance in this task requires coordinated generation of appropriate reach, to bring the hand to the target, and differentiated grasp, to preshape the hand congruent with object form. In Experiment 1, we tested PDPs in the off-medication state. To examine the dependence of subjects on visual feedback and their ability to implement intermodal sensory integration, we required them to reach and grasp the target objects in three conditions: (1) Full Vision, (2) Object Vision with only the target object visible and, (3) No Vision with neither the moving arm nor the target object visible. PDPs exhibited two types of deficits. First, in all conditions, they demonstrated a generalized slowing of movement or bradykinesia. We consider this an intensive deficit, since it involves largely a modulation of the gain of specific task parameters: in this case, velocity of movement. Second, they were less able than controls to extract critical proprioceptive information and integrate it with vision in order to coordinate the reach and grasp components of movement. These deficits which involve the coordination of different inputs and motor components, we classify as coordinative deficits. As in our previous work, the PDPs’ deficits were most marked when they were required to use proprioception to guide their hand to a visible target (Object Vision condition). But even in the full-vision condition, their performance only became fully accurate when both the target and effector (hand) were simultaneously visible. In Experiment 2, PDPs were tested on their dopaminergic replacement therapy. Dopaminergic treatment significantly ameliorated the bradykinesia of the PDPs, but produced no changes in the hand preshaping deficiencies of PDPs. These results suggest that adequate treatment of the PDPs may more readily compensate for intensive, than coordinative deficits, since the latter are likely to depend on specific and time-dependent neural interdependencies that are unlikely to be remediated simply by increasing the gain of a pathway.

The serial reaction time task revisited: a study on motor sequence learning with an arm-reaching task

With a series of novel arm-reaching tasks, we have shown that visuomotor sequence learning encompasses the acquisition of the order of sequence elements, and the ability to combine them in a single, skilled behavior. The first component, which is mostly declarative, is reflected by changes in movement onset time (OT); the second, which occurs without subject’s awareness, is measured by changes in kinematic variables, including movement time (MT). Key-press-based serial reaction time tasks (SRTT) have been used to investigate sequence learning and results interpreted as indicative of the implicit acquisition of the sequence order. One limitation to SRT studies, however, is that only one measure is used, the response time, the sum of OT and MT: this makes interpretation of which component is learnt difficult and disambiguation of implicit and explicit processes problematic. Here, we used an arm-reaching version of SRTT to propose a novel interpretation of such results. The pattern of response time changes we obtained was similar to the key-press-based tasks. However, there were significant differences between OT and MT, suggesting that both partial learning of the sequence order and skill improvement took place. Further analyses indicated that the learning of the sequence order might not occur without subjects’ awareness.

Influence of movement speed on accuracy and coordination of reaching movements to memorized targets in three-dimensional space in a deafferented subject

Multiarticular reaching movements at different speeds produce differential demands for the on-line control of ongoing movements and for the predictive control of intersegmental dynamics. The aim of this study was to assess the ability of a proprioceptively deafferented patient and aged-matched control subjects to make precise and coordinated three-dimensional reaching movements at different speeds without vision during the movement. A patient with a complete loss of proprioception below the neck (C.F.) and five control subjects made reaching movements to four remembered visual targets at slow, natural, and fast speeds. All movements were performed without vision of the arm during the movements. The spatial accuracy, the movement kinematics and the interjoint coordination of these movements were analyzed. Results showed that control subjects made larger spatial errors at both slow and fast speeds than at natural speed. However, they synchronized motions at the shoulder and elbow joints and kept most movement kinematic features invariant across speed conditions. In contrast, C.F. failed to produce smooth and simultaneous motions at the shoulder and elbow joints at all speeds. Surprisingly, however, he made much larger errors than control subjects at slow and natural speeds, but not at fast speed. Analysis of patterns of interjoint coordination revealed that, when instructed to move fast, C.F. initiated arm movements by fixing the elbow while moving the shoulder joint to damp interaction torques exerted on the elbow joint from motion of the upper arm. The results demonstrated that, although proprioceptive loss disrupted normal control of multijoint movements at all speeds, when performing relatively fast three-dimensional movements, C.F. could control intersegmental dynamics by reducing the number of active joints. More importantly, the results highlight the dual role of proprioception in controlling multijoint movements; that is, to provide important cues both for the predictive control of interaction torques and for the synchronization of adjacent joints even when interactive torques are very small. These findings support the idea that proprioceptive input is used by the CNS to update an internal model of limb dynamics that adapts the motor plan according to biomechanical contexts.

Differential Recruitment of Anterior Intraparietal Sulcus and Superior Parietal Lobule during Visually Guided Grasping Revealed by Electrical Neuroimaging

Dorsal parietal cortex is required for visually guided prehension. Transcranial magnetic stimulation to either the anterior intraparietal sulcus (aIPS) or superior parietal lobule (SPL) disrupts on-line adaptive adjustments of grasp when objects are perturbed. We used high-density electroencephalography during grasping to determine the relative timing of these two areas and to test whether the temporal contribution of each site would change when the task goal was perturbed. During object grasping with the right-hand, two distinct evoked responses were present over the 50–100 and 100–200 ms periods after movement onset. Distributed linear source estimation of these scalp potentials localized left lateralized sources, first in the aIPS and then the SPL. The duration of the response from the aIPS area was longer when there was an object perturbation. Initiation of a corrective movement coincided with activation in SPL. These data support a two-stage process: the integration of target goal and an emerging action plan within aIPS and subsequent on-line adjustments within SPL.

On-line grasp control is mediated by the contralateral hemisphere

Electrophysiological recordings from monkeys, as well as functional imaging and neuropsychological work with humans, have suggested that a region in the anterior portion of the intraparietal sulcus (aIPS) is involved in prehensile movements. With recent methodological advances using transcranial magnetic stimulation (TMS), we can now causally attribute anatomy with function to more precisely determine the specific involvement of aIPS in grasping. It has recently been demonstrated that aIPS is specifically involved in executing a grasp under conditions of both constant target requirements, as well as in correcting a movement under conditions in which a target perturbation occurs. In the present study, we extend these findings by determining the differential contribution of the left and right hemisphere to executing a grasping movement with the left and right hands. Transient disruption of left aIPS at movement onset impairs grasping with the right but not the left hand, and disruption of right aIPS impairs grasping with the left but not the right hand. We conclude that grasping is a lateralized process, relying exclusively on the contralateral hemisphere, and discuss the implications of these findings in relationship to models of hemispheric dominance for motor control.