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Rens, G.

Publications and source records attributed to Rens, G..

7 recordsLinked to original sources

Grasping with a twist: Dissociating action goals from motor actions in human frontoparietal circuits

In daily life, prehension is typically not the end goal of hand-object interactions but a precursor for manipulation. Nevertheless, functional MRI (fMRI) studies investigating manual manipulation have primarily relied on prehension as the end goal of an action. Here, we used slow event-related fMRI to investigate differences in neural activation patterns between prehension in isolation and prehension for object manipulation. Sixteen participants were instructed either to simply grasp the handle of a rotatable dial (isolated prehension) or to grasp and turn it (prehension for object manipulation). We used representational similarity analysis to investigate whether the experimental conditions could be discriminated from each other based on differences in task-related brain activation patterns. We also used temporal multivoxel pattern analysis to examine the evolution of regional activation patterns over time. Importantly, we were able to differentiate isolated prehension and prehension for manipulation from activation patterns in the early visual cortex, the caudal intraparietal sulcus, and the superior parietal lobule. Our findings indicate that object manipulation extends beyond the putative cortical grasping network (anterior intraparietal sulcus, premotor and motor cortices) to include the superior parietal lobule and early visual cortex. Significance statementA simple act such as turning an oven dial requires not only that the central nervous system encode the initial state (starting dial orientation) of the object but also the appropriate posture to grasp it in order to achieve the desired end state (final dial orientation) and the motor commands to achieve that state. Using advanced temporal neuroimaging analysis techniques, we reveal how such actions unfold over time and how they differ between object manipulation (turning a dial) vs. grasping alone. We find that a combination of brain areas implicated in visual processing and sensorimotor integration can distinguish between the complex and simple tasks during planning, with neural patterns that approximate those during the actual execution of the action.

neuroscience↗

The effect of type and context of sensorimotor information on corticospinal excitability

Fingertip force scaling during hand-object interactions typically relies on visual information about the object and sensorimotor memories from previous object interactions. Here, we investigated whether contextual information, that is not explicitly linked to the intrinsic object properties (e.g., size or weight) but is informative for motor control requirements, can mediate force scaling. For this, we relied on two separate behavioral tasks during which we applied transcranial magnetic stimulation (TMS) to probe corticospinal excitability (CSE), as a window onto the primary motor cortex role in controlling fingertip forces. In experiment 1, participants performed a force tracking task, where we manipulated available implicit and explicit visual information. That is, either the force target was fully visible, or only the force error was displayed as a deviation from a horizontal line. We found that participants performance was better when the former condition, in which they had explicit access to predictive information. However, we did not find differences in CSE modulation based on the type of visual information. On the other hand, CSE was modulated by the change in muscle contraction, i.e., contraction vs. relaxation and fast vs. slow changes. In sum, these findings indicate that CSE only reflects the ongoing motor command. In experiment 2, other participants performed a sequential object lifting task of visually identical objects that were differently weighted, in a seemingly random order. Within this task, we hid short series of incrementally increasing object weights. This allowed us to investigate whether participants would scale their forces for specific object weights based on the previously lifted object (i.e., sensorimotor effect) or based on the implicit information about the hidden series of incrementally increasing weights (i.e., extrapolation beyond sensorimotor effects). Results showed that participants did not extrapolate fingertip forces based on the hidden series but scaled their forces solely on the previously lifted object. Unsurprisingly, CSE was not modulated differently when lifting series of random weights versus series of increasing weights. Altogether, these results in two different grasping tasks suggest that CSE encodes ongoing motor components but not sensorimotor cues that are hidden within contextual information. HighlightsO_LIExplicit visual cues and sensorimotor experience are key for object grasping C_LIO_LIInvestigating influence of implicit, contextual information on object grasping C_LIO_LIExplicit but not implicit cues improve motor performance during object grasping C_LIO_LIExplicit but not implicit cues modulate corticospinal excitability C_LI

neuroscience↗

Motor resonance is modulated by an object's weight distribution

Transcranial magnetic stimulation (TMS) studies showed that corticospinal excitability (CSE) is modulated during observation of object lifting, an effect termed motor resonance. Specifically, motor resonance is driven by movement features indicating object weight, such as object size or observed movement kinematics. We investigated in 16 humans (8 females) whether motor resonance is also modulated by an objects weight distribution. Participants were asked to lift an inverted T-shaped manipulandum with interchangeable center of mass after first observing an actor lift the same manipulandum. Participants and actor were instructed to minimize object roll and rely on constrained digit positioning during lifting. Constrained positioning was either collinear (i.e., fingertips on the same height) or noncollinear (i.e., fingertip on the heavy side higher than the one on the light side). The center of mass changed unpredictably before the actors lifts and participants were explained that their weight distribution always matched the actors one. Last, TMS was applied during both lift observation and planning of lift actions. Our results showed that CSE was similarly modulated during lift observation and planning: when participants observed or planned lifts in which the weight distribution was asymmetrically right-sided, CSE recorded from the thumb muscles was significantly increased compared to when the weight distribution was left-sided. During both lift observation and planning, this increase seemed to be primarily driven by the weight distribution and not specifically by the (observed) digit positioning or muscle contraction. In conclusion, our results indicate that complex intrinsic object properties such as weight distributions can modulate activation of the motor system during both observation and planning of lifting actions. Highlights* Motor resonance is observation-induced activity in the observers motor system * We used a dyadic lifting task of objects with asymmetrical weight distribution * We investigated which movement features modulate motor resonance * Motor resonance is modulated by the objects weight distribution * Motor resonance is driven by observed and planned digit positioning

neuroscience↗

Lift observation conveys object weight distribution but partly enhances predictive lift planning

Observation of object lifting allows updating of internal object representations for object weight, in turn enabling accurate scaling of fingertip forces when lifting the same object. Here, we investigated whether lift observation also enables updating of internal representations for an objects weight distribution. We asked participants to lift an inverted T-shaped manipulandum, of which the weight distribution could be changed, in turns with an actor. Participants were required to minimize object roll (i.e., lift performance) during lifting and were allowed to place their fingertips at self-chosen locations. The center of mass changed unpredictably every third to sixth trial performed by the actor and participants were informed that they would always lift the same weight distribution as the actor. Participants observed either erroneous (i.e., object rolling towards its heavy side) or skilled (i.e., minimized object roll) lifts. Lifting performance after observation was compared to lifts without prior observation and to lifts after active lifting, which provided haptic feedback about the weight distribution. Our results show that observing both skilled and erroneous lifts convey an objects weight distribution similar to active lifting, resulting in altered digit positioning strategies. However, minimizing object roll on novel weight distributions was only improved after observing error lifts and not after observing skilled lifts. In sum, these findings suggest that although observing motor errors and skilled motor performance enables updating of digit positioning strategy, only observing error lifts enables changes in predictive motor control when lifting objects with unexpected weight distributions. New and noteworthyIndividuals are able to extract an objects size and weight by observing interactions with objects and subsequently integrate this information in their own motor repertoire. Here, we show that this ability extrapolates to weight distributions. Specifically, we highlighted that individuals can perceive an objects weight distribution during lift observation but can only partially embody this information when planning their own actions.

neuroscience↗

The role of the anterior intraparietal sulcus and the lateral occipital cortex in fingertip force scaling and weight perception during object lifting

Skillful object lifting relies on scaling fingertip forces according to the objects weight. When no visual cues about weight are available, force planning relies on recent lifting experience. Recently, we showed that previously lifted objects also affect weight estimation, as objects are perceived to be lighter when lifted after heavy objects compared to light ones. Here, we investigated the underlying neural mechanisms mediating these effects. We asked participants to lift objects and estimate their weight. Simultaneously, we applied transcranial magnetic stimulation (TMS) during the dynamic loading or static holding phase. Two subject groups received TMS of either the anterior intraparietal sulcus (aIPS) or lateral occipital area (LO), known to be important nodes in object grasping and perception. We hypothesized that TMS-induced disruption of aIPS and LO would alter force scaling and weight perception. Contrary to our hypothesis, we did not find effects of aIPS or LO stimulation on force planning or weight estimation caused by previous lifting experience. However, we found that TMS of both areas increased grip forces, but only when applied during dynamic loading, and decreased weight estimation, but only when applied during static holding, suggesting time-specific effects. Interestingly, our results also indicate that TMS over LO, but not aIPS, affected load force scaling specifically for heavy objects, which further indicates that planning of load and grip forces might be controlled differently. These findings provide new insights on the interactions between brain networks mediating action and perception during object manipulation. NEW & NOTEWORTHYThis article provides new insights into the neural mechanisms underlying object lifting and perception. Using transcranial magnetic stimulation during object lifting, we show that effects of previous experience on force scaling and weight perception are not mediated by the anterior intraparietal sulcus nor the lateral occipital cortex (LO). In contrast, we highlight a unique role for LO in load force scaling, suggesting different brain processes for grip and load force scaling in object manipulation.

neuroscience↗

Sensorimotor expectations bias motor resonance during observation of object lifting: The causal role of pSTS

Transcranial magnetic stimulation (TMS) studies have highlighted that corticospinal excitability (CSE) is increased during observation of object lifting, an effect termed motor resonance. This facilitation is driven by movement features indicative of object weight, such as object size or observed movement kinematics. Here, we investigated in 35 humans (23 females) how motor resonance is altered when the observers weight expectations, based on visual information, do not match the actual object weight as revealed by the observed movement kinematics. Our results highlight that motor resonance is not robustly driven by object weight but easily masked by a suppressive mechanism reflecting the correctness of the weight expectations. Subsequently, we investigated in 24 humans (14 females) whether this suppressive mechanism was driven by higher-order cortical areas. For this, we induced virtual lesions to either the posterior superior temporal sulcus (pSTS) or dorsolateral prefrontal cortex (DLPFC) prior to having participants perform the task. Importantly, virtual lesion of pSTS eradicated this suppressive mechanism and restored object weight-driven motor resonance. In addition, DLPFC virtual lesion eradicated any modulation of motor resonance. This indicates that motor resonance is heavily mediated by top-down inputs from both pSTS and DLPFC. Altogether, these findings shed new light on the theorized cortical network driving motor resonance. That is, our findings highlight that motor resonance is not only driven by the putative human mirror neuron network consisting of the primary motor and premotor cortices as well as the anterior intraparietal sulcus, but also by top-down input from pSTS and DLPFC. Significance StatementObservation of object lifting activates the observers motor system in a weight-specific fashion: Corticospinal excitability is larger when observing lifts of heavy objects compared to light ones. Interestingly, here we demonstrate that this weight-driven modulation of corticospinal excitability is easily suppressed by the observers expectations about object weight and that this suppression is mediated by the posterior superior temporal sulcus. Thus, our findings show that modulation of corticospinal excitability during observed object lifting is not robust but easily altered by top-down cognitive processes. Finally, our results also indicate how cortical inputs, originating remotely from motor pathways and processing action observation, overlap with bottom-up motor resonance effects.

neuroscience↗

The observation of explicit and implicit visuomotor cues can drive predictive motor control

Recent studies have highlighted that the observation of hand-object interactions can influence perceptual weight judgements made by an observer. Moreover, observing explicit motor errors during object lifting allows individuals to update their internal sensorimotor representation about object weight. Embodying observed visuomotor cues for the planning of a motor command further enables individuals to accurately scale their fingertip forces when subsequently lifting the same object. However, it is still unknown whether observation of a skilled lift is equally able to mediate predictive motor control in the observer. Here, we tested this hypothesis by asking participants to grasp and lift a manipulandum after observing an actors lift. The object weight changed unpredictably (light or heavy) every third to sixth trial performed by the actor. Participants were informed that they would always lift the same weight as the actor and that, based on the experimental condition, they would have to observe skilled or erroneously performed lifts. Our results revealed that the observation of both skilled and erroneously performed lifts allows participants to update their internal sensorimotor object representation, in turn enabling them to predict force scaling accurately. These findings suggest that the observation of explicit as well as implicit visuomotor cues are embodied in the observers motor repertoire and can drive changes in predictive motor control.

neuroscience↗